Histopathological changes in the gills of zebrafish (Danio rerio) and bullfrog tadpoles (Lithobates catesbeianus) caused by the use of formaldehyde / Alterações histopatológicas em brânquias de peixe-zebra (Danio rerio) e girinos de rã-touro (Lithobates catesbeianus) causada pelo uso de formaldeído

Autores

  • Diego Sales Santos Brazilian Journals Publicações de Periódicos, São José dos Pinhais, Paraná
  • Fernanda Menezes França
  • Adriana Sacioto Marcantonio
  • Cristina Viriato
  • Ana Maria Cristina Rebello Pinto Fonseca Martins
  • Cintia Badaró Pedroso
  • Cláudia Maris Ferreira

DOI:

https://doi.org/10.34188/bjaerv4n3-090

Palavras-chave:

Anurans. Branchial arches. Formalin. Histological damage. Osteichthyes.

Resumo

Formaldehyde is a carcinogenic and aggressive agent mainly to epithelial tissues. However, for rearing aquatic organisms its use is common for the treatment of fungi and parasites, and the use of incorrect doses can harm the health and life of these animals. The fish species Danio rerio and the tadpoles of the species Lithobates catesbeianus are internationally recognized for use in aquatic toxicology tests. We aimed identify the effects caused by formaldehyde on the gills of these two experimental models used in aquatic toxicology, verifying the susceptibility of both species. Acute and chronic tests with formaldehyde were conducted for experiment. We found that the formaldehyde in the higher concentration caused injuries to the gills of both fish and tadpoles, with a loss and displacement of epithelium, vascular congestion, telangiectasia and lamellar epithelial lifting/edema (possible aneurysm), hyperplasia and hypertrophy of epithelial cells, lamellar fusion in addition to the proliferation of mucus-secreting cells and chloride cells. Despite structural differences, the histological changes caused by chronic exposure to formaldehyde in sublethal concentrations were similar in both organisms and we recommend reviewing its use in prophylaxis and in prolonged treatments with this chemical.

Referências

ABNT - Associação Brasileira de Normas Técnicas. NBR 15088. Ecotoxicologia aquática – Toxicidade aguda. Método de ensaio com peixes. São Paulo, 2016, p.19.

APHA; AWWA; WPCF. Standard methods for the examination of water and wastewater. 20a. ed., Washington DC. 2005.

ASTM - American Society For Testing And Materials. Standard guide for conducting acute toxicity tests on test materials with fishes, macroinvertebrates and amphibians. West Conshohocken, PA, 2014, p 218-238.

Bandara MGDK, Wijesinghe MR, Ratnasooriya WD, Priyani AAH Chlorpyrifos-induced histopathological alterations in Duttaphrynus melanostictus (Schneider 1799) tadpoles: evidence from empirical trials. J Trop For Sci. 2012; 2: 27-36. http://doi:10.31357/jtfe.v2i2.592.

Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell JA, Mcpherson JD, Johnson SL The syntenic relationship of the zebrafish and human genomes. Genome Res. 2000; 10: 1351-1358. https://doi:10.1101/gr.144700.

Bueno-Guimarães, HM, Ferreira CM, Garcia MLB, Saldiva PHN Tadpole epithelium test: potential use of Rana catesbeiana histopathologic epithelial changes to evaluate aquatic pollution. Bull Environ Contam Toxicol 2001; 67: 202-209. https://doi:10.1007/s001280111.

CONCEA 2014. Resolução Normativa no 17. https://www.mctic.gov.br/mctic/opencms/institucional/concea/paginas/legislacao. Accessed 6 August 2019.

Cribb AY, Afonso AM, Mostério CMF Manual técnico de ranicultura. Embrapa, Brasília, 2013.73p.

Cruz C, Fujimoto RY, Luz RK, Portella MC, Martins ML Toxicidade aguda e histopatologia do fígado de larvas de trairão Hoplias lacerdae expostas à solução aquosa de formaldeído a 10%. Pesticidas: Rev. Ecotoxicologia e Meio Ambiente 2005; 15: 21-28. https://doi.org/10.5380/pes.v15i0.4502.

De Swaef E, Den Broeck WV, Dierckens K, Decostere A Disinfection of teleost eggs: a review. Aquaculture 2015; 7: 1–21. https://doi.org/10.1111/raq.12096.

Devaraj P, Babu V, Cengiz EI Qualitative detection of formaldehyde and ammonia in fish and other seafoods obtained from Chennai's (India) fish markets. Environ Monit Assess. 2021; 193(2):78. https://doi.org/10.1007/s10661-021-08871-z.

ECOTOX Data Base. 2006. Avaible in: https://cfpub.epa.gov/ecotox. Accessed in May 2018.

Erkmen B, Kolankaya D Effects of water quality on epithelial morphology in the gill of Capoeta tinca living in two tributaries of K?z?l?rmak River, Turkey. Bull Environ Contam Toxicol. 2000; 64: 418-425. https://doi.org/10.1007/s001280000017.

Evans JJ, Klesius PH, Shoemaker CA Therapeutic and prophylactic immunization against Streptococcus iniae infection in hybrid striped bass (Morone chrysops × Morone saxatilis). Aquac Res. , 2006; 37: 742-750. https://doi.org/10.1111/j.1365-2109.2006.01487.x.

França FM, Brazil De Paiva TC, Marcantônio AS, Teixeira PC, Ferreira CM Acute toxicity and ecotoxicological risk assessment of rice pesticides to Lithobates catesbeianus tadpoles. J Environ Sci Heal B. 2015; 50: 406-410. https://doi.org/10.1080/03601234.2015.1011950.

Frost DR Amphibian Species of the World. American Museum of Natural History. New York. 2016. Avaible in: http://research.amnh.org/vz/herpetology/amphibia/index.html. Accessed 21 May 2019.

Gomez Isaza DF, Cramp RL, Franklin CE Living in polluted waters: A meta-analysis of the effects of nitrate and interactions with other environmental stressors on freshwater taxa. Environ Pollut. 2020; 114091. https://doi.org/10.1016/j.envpol.2020.114091.

Gosner KL A simplified table for standing anuran embryos and larvae with notes on identification. Herpetologica 1960; 16: 183-190.

Hamilton MA, Russo RC, Thurston RV Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol. 1977; 11: 714-719. https://doi.org/10.1021/es60130a004.

Hermenean A, Damache G, Albu P, Ardelean A, Ardelean G, Puiu Ardelean D, Horge M, Nagy T, Braun M, Zsuga M, Kéki S, Costache M, Dinischiotu A Histopatological alterations and oxidative stress in liver and kidney of Leuciscus cephalus following exposure to heavy metals in the Tur River, North Western Romania. Ecotoxicol Environ Saf. 2015; 119: 198-205.

Hohreiter DW, Rigg DK Derivation of ambient water quality criteria for formaldehyde. Chemosphere 2001; 45: 471-486. https://doi.org/1016/S0045-6535(01)00061-3.

IARC - International Agency for Research on Cancer, World Health Organization. IARC Monographs on the Evalution of Carcinogenic Risks to Humans. 2014. 88, 483. http://monographs.iarc.fr/ENG/Monographs/vol88/index.php. Accessed 21 May 2019.

Leal JF, Neves MGPMS, Santos EBH, Esteves VI Use of formalin in intensive aquaculture: properties, application and effects on fish and water quality. Rev Aquacult. 2018; 10: 281–229. https://doi.org/10.1111/raq.12160.

Linde-Arias AR, Inácio AF, de Alburquerque C, Freire MM, Moreira JC Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian River Sci Total Environ. 2008; 399: 186-192. https://doi.org/10.1016/j.scitotenv.2008.03.028.

Liu TT, Hou H, Du JL A protocol for simultaneous Ca2+ and morphology imaging of brain endothelial tip cells in larval zebrafish. STAR Protoc. 2021; 2(1):100388. https://doi.org/10.1016/j.xpro.2021.100388.

Lombardi JV, Perpetuo TR, Ferreira CM, Machado-Neto JG, Marques HLA Acute toxicity of the fungicide copper oxychloride to tadpoles of the bullfrog Rana catesbeiana. Bull Environ Contam Toxicol. 2002; 69: 415-420. https://doi.org/10.1007/s00128-002-0078-6.

Machado MR, Fanta E Effects of the organophosphorous methyl parathion on the branchial epithelium of a freshwater fish Metynnis roosevelti. Braz Arch Biol Technol. 2003; 46: 361-372. https://doi.org/10.1590/S1516-89132003000300008.

Magare SR, Patil HT Effect of pesticides on oxygen consumption, red blood cell count and metabolites of a fish, Puntius ticto. Environ Ecology 2000; 18: 891-894.

Martins ML Cuidados básicos e alternativas no tratamento de enfermidades de peixes na aquicultura brasileira. In: Ranzani-Paiva MJ, Takemoto RM, Lizama MAP (eds.). Sanidade de Organismos Aquáticos, São Paulo: Editora Varela, 2004, p. 355-368

McDonald DG, Wood CM Branchial mechanisms of acclimation to metals in freshwater fish. In Fish ecophysiology. Springer, Dordrecht, 1993, p. 297-321.

Motais R, Garcia-Romeu F Transport mechanisms in the teleostean gill and amphibian skin. Annu Rev Physiol. 1972; 34: 141-76. https://doi.org/10.1146/annurev.ph.34.030172.001041.

Noga EJ Fish Disease: Diagnosis and Treatment. Iowa: Wiley-Blackwell. 2010. 378p.

Ogbeide O, Uhunamure G, Uwagboe L, Osakpamwan T, Glory M, Chukwuka A Comparative gill and liver pathology of Tilapia zilli, Clarias gariepinus and Neochanna diversus in owan river (Nigeria): Relative ecological risks of species in a pesticide impacted river. Chemosphere 2019; 234: 1-13. https://doi.org/10.1016/j.chemosphere.2019.06.055.

Pahor?Filho E, Miranda Filho KC, Klosterhoff M, Romano LA, Pereira Júnior J Histopathological and behaviour effects of formaldehyde treatment in juvenile mullet, Mugil liza (Valenciennes). Aquac Res. 2015; 46: 3040-3045. https://doi.org/10.1111/are.12462.

Paixão LF, Santos RFB, Ramos FM, Fujimoto RY Efeitos do tratamento com formalina e sulfato de cobre sobre os parâmetros hematológicos e parasitos monogenéticos em juvenis de Hemigrammus sp. (Osteichthyes: Characidae). Acta Amazonica 2013; 43: 211-216.

Ramos T, Romano LA, Pereira JRJ Evolução histopatológica em brânquias de tainhas Mugil liza expostas à banhos terapêuticos com formalina. Rev Bras Engenharia de Pesca 2014; 7: 45-59. https://doi.org/10.18817/repesca.v7i1.1064.

Randall DJ, Tsui TKN Ammonia toxicity in fish. Mar Pollut Bull. 2002; 45: 17-23. https://doi.org/10.1016/S0025-326X(02)00227-8.

Resendes AS, Santos DS, França FM, Petesse ML, Badaró-Pedroso C, Ferreira CM Acute toxic and genotoxic effects of formalin in Danio rerio (zebrafish). Ecotoxicology 2018; 27:1379-1386. https://doi.org/10.1007/s10646-018-1993-6.

Russel, W.M.S., Burch, R.L., 1959. The Principles of Humane Experimental Technique, Methuen, London, Johns Hopkins University, Baltimore.

Saltys HA, Jonz MG, Nurse CA Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell Tissue Res. 2006; 323: 1–10. https://doi.org/10.1007/s00441-005-0048-5.

Santana JM, Dos Reis A, Teixeira PC, Ferreira FC, Ferreira CM Median lethal concentration of formaldehyde and its genotoxic potential in bullfrog tadpoles (Lithobates catesbeianus). J Environ Sci Heal B. 2015;50: 896-900. https://doi.org/10.1080/03601234.2015.1067095.

Santos EF, Tavares-Dias M, Pinheiro DA, Neves LR, Marinho RGB, Dias MKR Fauna parasitária de tambaqui Colossoma macropomum (Characidae) cultivado em tanque-rede no estado do Amapá, Amazônia oriental. Acta Amazonica 2013; 43: 105 – 112.

Spitsbergen JM, Kent ML The state of the art of the zebrafish model for toxicology and toxicologic pathology research–advantages and current limitations. Toxicol Pathology 2003; 31 (Suppl.): 62–87. https://doi.org/10.1080/01926230390174959.

Teraoka H, Dong W, Tsujimoto Y, Iwasa H, Endoh D, Ueno N, Stegeman JJ, Peterson RE, Hiraga T Induction of cytochrome P450 1A is required for circulation failure and edema by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in zebrafish. Biochem Biophys Res Commun. 2003; 304: 223-228. https://doi.org/10.1016/S0006-291X(03)00576-X.

Thushari GGN, Senevirathna JDM Plastic pollution in the marine environment. Heliyon. 2020; 6(8):04709. https://doi: 10.1016/j.heliyon.2020.e04709.

Viriato C, França FM, Santos DS, Marcantonio AS, Badaró-Pedroso C, Ferreira CM Evaluation of the potential teratogenic and toxic effect of the herbicide 2,4-D (DMA® 806) in bullfrog embryos and tadpoles (Lithobates catesbeianus). Chemosphere 2020; 266:129018. https://doi.org/10.1016/j.chemosphere.2020.129018.

Wong CK, Wong MH Morphological and biochemical changes in the gills of tilapia (Oreochromis mossambicus) to ambient cadmium exposure. Aquat Toxicol. 2000; 48: 517-527. https://doi.org/10.1016/S0166-445X(99)00060-0.

Wood CM, Eom J The osmorespiratory compromise in the fish gill. Comp Biochem Physiol A Mol Integr Physiol. 2021; 254: 110895. https://doi.org/10.1016/j.cbpa.2021.110895.

Zhang Y, Feng J, Gao Y,Liu X, Qu L, Zhu L Physiologically based toxicokinetic and toxicodynamic (PBTK-TD) modelling of Cd and Pb exposure in adult zebrafish Danio rerio: Accumulation and toxicity. Environ Pollut 2019; 249: 959-968.https://doi: 10.1016/j.envpol.2019.03.115.

Zagatto PA, Bertoletti E. Ecotoxicologia Aquática – Princípios e Aplicações. 2ª Ed. São Carlos: Rima. 2008. 486 p.

Zar JH Biostatical Analysis. Prentice Hall, New Jersey. Prentice. 1999. 946p.

Downloads

Publicado

2021-08-25

Como Citar

Santos, D. S., França, F. M., Marcantonio, A. S., Viriato, C., Martins, A. M. C. R. P. F., Pedroso, C. B., & Ferreira, C. M. (2021). Histopathological changes in the gills of zebrafish (Danio rerio) and bullfrog tadpoles (Lithobates catesbeianus) caused by the use of formaldehyde / Alterações histopatológicas em brânquias de peixe-zebra (Danio rerio) e girinos de rã-touro (Lithobates catesbeianus) causada pelo uso de formaldeído. Brazilian Journal of Animal and Environmental Research, 4(3), 3832–3847. https://doi.org/10.34188/bjaerv4n3-090

Edição

Seção

Artigos originais