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Research Article

Effect of short-term exposure to low concentration of tebuconazole: morphological, histometric and functional modifications in Danio rerio liver

ORCID Icon, , , & ORCID Icon
Pages 331-345 | Received 13 Dec 2021, Accepted 13 Feb 2022, Published online: 09 Mar 2022

References

  • Altenhofen S, Nabinger DD, Wiprich MT, Pereira TCB, Bogo MR, Bonan CD. 2017. Tebuconazole alters morphological, behavioral and neurochemical parameters in larvae and adult zebrafish (Danio rerio). Chemosphere 180:483–490. DOI: 10.1016/j.chemosphere.2017.04.029.
  • American Society for Testing and Materials (ASTM). 2002. Standard guide for conducting acute toxicity test with fishes, macroinvertebrates, and amphibians E 729 - 96. In: Annual book of ASTM standards. Philadelphia (PA). pp. 165–174.
  • Andreu‐Sánchez O, Paraíba LC, Jonsson CM, Carrasco JM. 2011. Acute toxicity and bioconcentration of fungicide tebuconazole in zebrafish (Danio rerio). Environmental Toxicology 27:109–116. DOI: 10.1002/tox.20618.
  • Avdesh A, Chen M, Martin-Iverson MT, Mondal A, Ong D, Rainey-Smith S, Taddei K, Lardelli M, Groth DM, Verdile G, Martins RN. 2012. Regular care and maintenance of a zebrafish (Danio rerio) laboratory: An introduction. The Journal of Visualized Experiments 69:e4196. DOI: 10.3791/4196.
  • Bernabò I, Guardia A, Macirella R, Sesti S, Tripepi S, Brunelli E. 2020. Tissues injury and pathological changes in Hyla intermedia juveniles after chronic larval exposure to tebuconazole. Ecotoxicology and Environmental Safety 205:111367. DOI: 10.1016/j.ecoenv.2020.111367.
  • Bernabò I, Guardia A, Macirella R, Tripepi S, Brunelli E. 2017. Chronic exposures to fungicide pyrimethanil: Multi-organ effects on Italian tree frog (Hyla intermedia). Scientific Reports 7:6869. DOI: 10.1038/s41598-017-07367-6.
  • Biller-Takahashi JD, Urbinati EC. 2014. Fish Immunology. The modification and manipulation of the innate immune system: Brazilian studies. Anais da Academia Brasileira de Ciências 86:1484–1506. DOI: 10.1590/0001-3765201420130159.
  • Biller JD, Takahashi LS. 2018. Oxidative stress and fish immune system: Phagocytosis and leukocyte respiratory burst activity. Anais da Academia Brasileira de Ciências 90:3403–3414. DOI: 10.1590/0001-3765201820170730.
  • Bonomo MM, de Castro Sachi IT, Paulino MG, Fernandes JB, Carlos RM, Fernandes MN. 2021. Multi-biomarkers approach to access the impact of novel metal-insecticide based on flavonoid hesperidin on fish. Environmental Pollution 268:115758. DOI: 10.1016/j.envpol.2020.115758.
  • Boran H, Capkin E, Altinok I, Terzi E. 2012. Assessment of acute toxicity and histopathology of the fungicide captan in rainbow trout. Experimental and Toxicologic Pathology 64:175–179. DOI: 10.1016/j.etp.2010.08.003.
  • Chang Y, Mao L, Zhang L, Zhang Y, Jiang H. 2020. Combined toxicity of imidacloprid, acetochlor, and tebuconazole to zebrafish (Danio rerio): Acute toxicity and hepatotoxicity assessment. Environmental Science and Pollution Research 27:10286–10295. DOI: 10.1007/s11356-020-07653-3.
  • Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, Yi J, Ryu DY. 2010. Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquatic Toxicology 100:151–159. DOI: 10.1016/j.aquatox.2009.12.012.
  • Çilingir Yeltekin A, Oğuz A, Kankaya E, Özok N, Güneş İ. 2020. Hematological and biochemical response in the blood of Alburnus tarichi (actinopterygii: cypriniformes: cyprinidae) exposed to tebuconazole. Acta Ichthyologica et Piscatoria 50:373–379. DOI: 10.3750/aiep/02931.
  • Clasen B, Loro VL, Murussi CR, Tiecher TL, Moraes B, Zanella R. 2018. Bioaccumulation and oxidative stress caused by pesticides in Cyprinus carpio reared in a rice-fish system. Science of the Total Environment 626:737–743. DOI: 10.1016/j.scitotenv.2018.01.154.
  • de Souza RM, Seibert D, Quesada HB, de Jesus Bassetti F, Fagundes-Klen MR, Bergamasco R. 2020. Occurrence, impacts, and general aspects of pesticides in surface water: A review. Process Safety and Environmental 135:22–37. DOI: 10.1016/j.psep.2019.12.035.
  • European Commission. 2020a. Pesticides. Available: https://ec.europa.eu/food/plant/pesticides_en. Accessed Mar 1 2021.
  • European Commission. 2020b. Sales of pesticides in the E.U. Available: https://ec.europa.eu/eurostat/web/products-eurostat-news/-/DDN-20200603-1 Accessed Feb 2021 25.
  • European Union. 2015. Implementing Regulation (E.U.) 2015/408 of 11.3.2015 on implementing Article 80 (7) of Regulation (E.C.) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection products on the market and establishing a list of candidates for substitution. Official Journal of European Union L. 67:18–22.
  • Ferreira D, da Motta AC, Kreutz LC, Toni C, Loro VL, Barcellos LJG. 2010. Assessment of oxidative stress in Rhamdia quelen exposed to agrichemicals. Chemosphere 79:914–921. DOI: 10.1016/j.chemosphere.2010.03.024.
  • Ferreira D, Unfer TC, Rocha HC, Kreutz LC, Koakoski G, Barcellos LJG. 2012. Antioxidant activity of bee products added to water in tebuconazole-exposed fish. Neotropical Ichthyology 10:215–220. DOI: 10.1590/S1679-62252012000100021.
  • Food and Agriculture Organization of the United Nations 2018. Database collection of the Food and Agriculture Organization of the United Nations. Available online: http://www.fao.org/faostat/en/#data. Accessed Feb 19 2021.
  • Fustinoni S, Mercadante R, Polledri E, Rubino FM, Mandic-Rajcevic S, Vianello G, Colosio C, Moretto A. 2014. Biological monitoring of exposure to tebuconazole in winegrowers. Journal of Exposure Science and Environmental Epidemiology 24:643–649. DOI: 10.1038/jes.2014.14.
  • Georgieva E, Yancheva V, Stoyanova S, Velcheva I, Iliev I, Vasileva T, Bivolarski B, Petkova E, László B, Nyeste K, Antal L. 2021. Which is more toxic? Evaluation of the short-term toxic effects of chlorpyrifos and cypermethrin on selected biomarkers in common carp (Cyprinus carpio, Linnaeus 1758). Toxics 9:125. DOI: 10.3390/toxics9060125.
  • Gharaei A, Ghaffari M, Keyvanshokooh S, Akrami R. 2011. Changes in metabolic enzymes, cortisol and glucose concentrations of Beluga (Huso huso) exposed to dietary methylmercury. Fish Physiology and Biochemistry 37:485–493. DOI: 10.1007/s10695-010-9450-3.
  • Grattagliano I, Bonfrate L, Diogo CV, Wang HH, Wang DQ, Portincasa P. 2009. Biochemical mechanisms in drug-induced liver injury: Certainties and doubts. World Journal of Gastroenterology 15:4865. DOI: 10.3748/wjg.15.4865.
  • Hvězdová M, Kosubová P, Košíková M, Scherr KE, Šimek Z, Brodský L, Šudoma M, Škulcová L, Sáňka M, Svobodová M, Krkošková L. 2018. Currently and recently used pesticides in Central European arable soils. Science of the Total Environment 613:361–370. DOI: 10.1016/j.scitotenv.2017.09.049.
  • Krewski D, Acosta JD, Andersen M, Anderson H, Bailar JC, Boekelheide K, Brent R, Charnley G, Cheung VG, Green JS, Kelsey KT, Kerkvliet NI, Li AA, McCray L, Meyer O, Patterson RD, Pennie W, Scala RA, Solomon GM, Stephens M, Yager J, Zeise L. 2010. Staff of Committee on Toxicity Testing and Assessment of Environmental Agents. Toxicity testing in the 21st century: A vision and a strategy. Journal of Toxicology and Environmental Health, Part B: Critical Reviews 13:51–138. DOI: 10.1080/10937404.2010.483176.
  • La Russa D, Marrone A, Mandalà M, Macirella R, Pellegrino D. 2020. Antioxidant/Anti-Inflammatory effects of caloric restriction in an aged and obese rat model: The role of adiponectin. Biomedicines 8:532. DOI: 10.3390/biomedicines8120532.
  • La Russa D, Montesano D, Pellegrino D, Frisina M, Bagetta G, Fallarino F, Amantea D. 2021. Systemic administration of sunflower oil exerts neuroprotection in a mouse model of transient focal cerebral ischaemia. Journal of Pharmacy and Pharmacology 22:rgab007. DOI: 10.1093/jpp/rgab007.
  • Li S, Jiang Y, Sun Q, Coffin S, Chen L, Qiao K, Gui W, Zhu G. 2020. Tebuconazole induced oxidative stress related hepatotoxicity in adult and larval zebrafish (Danio rerio). Chemosphere 241:125129. DOI: 10.1016/j.chemosphere.2019.125129.
  • Li S, Sun Q, Wu Q, Gui W, Zhu G, Schlenk D. 2019. Endocrine disrupting effects of tebuconazole on different life stages of zebrafish (Danio rerio). Environmental Pollution 249:1049–1059. DOI: 10.1016/j.envpol.2019.03.067.
  • Liu N, Dong F, Xu J, Liu X, Zheng Y. 2016. Chiral bioaccumulation behavior of tebuconazole in the zebrafish (Danio rerio). Ecotoxicology and Environmental Safety 126:78–84. DOI: 10.1016/j.ecoenv.2015.12.007.
  • Lutnicka H, Bojarski B, Ludwikowska A, Wrońska D, Kamińska T, Szczygieł J, Troszok A, Szambelan K, Formicki G. 2016. Hematological alterations as a response to exposure to selected fungicides in common carp (Cyprinus carpio L.). Folia Biol-Krakow 64:235–244. DOI: 10.3409/fb64_4.235.
  • Lv X, Pan L, Wang J, Lu L, Yan W, Zhu Y, Xu Y, Guo M, Zhuang S. 2017. Effects of triazole fungicides on androgenic disruption and CYP3A4 enzyme activity. Environmental Pollution 222:504–512. DOI: 10.1016/j.envpol.2016.11.051.
  • Macirella R, Guardia A, Pellegrino D, Bernabò I, Tronci V, Ebbesson LO, Sesti S, Tripepi S, Brunelli E. 2016. Effects of two sublethal concentrations of mercury chloride on the morphology and metallothionein activity in the liver of zebrafish (Danio rerio). International Journal of Molecular Sciences 17:361. DOI: 10.3390/ijms17030361.
  • Macirella R, Tripepi M, Brunelli E. 2019. Morphological and immunohistochemical modifications in Zebrafish (Danio rerio) gills after short-term exposure to the fungicide tebuconazole. Zebrafish 16:65–76. DOI: 10.1089/zeb.2018.1638.
  • Maggi F, Tang FHM, la Cecilia D, McBratney A. 2019. PEST-CHEMGRIDS, global gridded maps of the top 20 crop-specific pesticide application rates from 2015 to 2025. Science Data 170:1–20. DOI: 10.1038/s41597-019-0169-4.
  • Marcon L, Bazzoli N, Honor Mounteer A, Anjos Benjamin LD. 2015. Histological and histometric evaluation of the liver in Astyanax bimaculatus (Teleostei: Characidae), exposed to different concentrations of an organochlorine insecticide. The Anatomical Record 298:1754–1764. DOI: 10.1002/ar.23196.
  • Narra MR. 2016. Single and cartel effect of pesticides on biochemical and haematological status of Clarias batrachus: A long-term monitoring. Chemosphere 144:966–974. DOI: 10.1016/j.chemosphere.2015.09.065.
  • Nowak BF, Kingsford MJ. 2003. Exposure to Thiodan® results in lipofuscin accumulation in hepatocytes of the freshwater catfish Tandanus tandanus. Diseases of Aquatic Organisms 56:135–143. DOI: 10.3354/dao056135.
  • Ostaszewska T, Śliwiński J, Kamaszewski M, Sysa P, Chojnacki M. 2018. Cytotoxicity of silver and copper nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Environmental Science and Pollution Research 25:908–915. DOI: 10.1007/s11356-017-0494-0.
  • Othmène YB, Hamdi H, Salem IB, Annabi E, Amara I, Neffati F, Najjar MF, Abid-Essefi S. 2020. Oxidative stress, DNA damage and apoptosis induced by tebuconazole in the kidney of male Wistar rat. Chemico-Biological Interactions 330:109114. DOI: 10.1016/j.cbi.2020.109114.
  • Pal S, Kokushi E, Koyama J, Uno S, Ghosh AR. 2012. Histopathological alterations in gill, liver and kidney of common carp exposed to chlorpyrifos. Journal of Environmental Science and Health, Part B 47:180–195. DOI: 10.1080/03601234.2012.632285.
  • Paulo DV, Fontes FM, Flores-Lopes F. 2012. Histopathological alterations observed in the liver of Poecilia vivipara (Cyprinodontiformes: Poeciliidae) as a tool for the environmental quality assessment of the Cachoeira River, BA. Brazilian Journal of Biology 72:131–140. DOI: 10.1590/S1519-69842012000100015.
  • Pereira BF, Alves RDS, Alves AL, Senhorini JA, Rocha RCGA, Scalize PH, Pitol DL, Caetano FH. 2014. Effects of biodegradable detergents in morphological parameters of liver in two neotropical fish species (Prochilodus lineatus and Astyanax altiparanae). Microscopy Research 2:39–49. DOI: 10.4236/mr.2014.22006.
  • Perez-Rodriguez V, Souders CL, Tischuk C, Martyniuk CJ. 2019. Tebuconazole reduces basal oxidative respiration and promotes anxiolytic responses and hypoactivity in early-staged zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 217:87–97. DOI: 10.1016/j.cbpc.2018.11.017.
  • Qiu L, Jia K, Huang L, Liao X, Guo X, Lu H. 2019. Hepatotoxicity of tricyclazole in zebrafish (Danio rerio). Chemosphere 232:171–179. DOI: 10.1016/j.chemosphere.2019.05.159.
  • Rabitto IS, Costa JA, De Assis HS, Pelletier E, Akaishi FM, Anjos A, Randi MAF, Ribeiro CO. 2005. Effects of dietary Pb (II) and tributyltin on neotropical fish, Hoplias malabaricus: Histopathological and biochemical findings. Ecotoxicology and Environmental Safety 60:147–156. DOI: 10.1016/j.ecoenv.2004.03.002.
  • Rani M, Shanker U. 2018. Removal of chlorpyrifos, thiamethoxam, and tebuconazole from water using green synthesized metal hexacyanoferrate nanoparticles. Environmental Science and Pollution Research 25:10878–10893. DOI: 10.1007/s11356-018-1346-2.
  • Research and Markets. 2020. Global SDHI Fungicide Market - Forecasts from 2020 to 2025. Report ID 5215212. Available: https://www.researchandmarkets.com/reports/5215212/global-sdhi-fungicide-market-forecasts-from. Accessed March 10 2021.
  • Sadauskiene I, Liekis A, Staneviciene I, Naginiene R, Ivanov L. 2020. Effects of long-term supplementation with aluminum or selenium on the activities of antioxidant enzymes in mouse brain and liver. Catalysts 10:585. DOI: 10.3390/catal10050585.
  • Silva V, Mol HG, Zomer P, Tienstra M, Ritsema CJ, Geissen V. 2019. Pesticide residues in European agricultural soils - A hidden reality unfolded. Science of the Total Environment 653:1532–1545. DOI: 10.1016/j.scitotenv.2018.10.441.
  • Škulcová L, Neuwirthová N, Šimek Z, Trojan M, Bielská L. 2020. Enantioselective behavior of the fungicide tebuconazole in soil. Environmental Processes 7:173–188. DOI: 10.1007/s40710-019-00409-3.
  • Stephenie S, Chang YP, Gnanasekaran A, Esa NM, Gnanaraj C. 2020. An insight on superoxide dismutase (SOD) from plants for mammalian health enhancement. Journal of Functional Foods 68:103917. DOI: 10.1016/j.jff.2020.103917.
  • Stoyanova S, Georgieva E, Velcheva I, Iliev I, Vasileva T, Bivolarski V, Tomov S, Nyeste K, Antal L, Yancheva V. 2020. Multi-biomarker assessment in common carp (Cyprinus carpio, Linnaeus 1758) liver after acute chlorpyrifos exposure. Water 12:1837. DOI: 10.3390/w12061837.
  • Šudoma M, Peštálová N, Bilkova Z, Sedláček P, Hofman J. 2021. Ageing effect on conazole fungicide bioaccumulation in arable soils. Chemosphere 262:127612. DOI: 10.1016/j.chemosphere.2020.127612.
  • Tabassum H, Dawood AQ, Sharma P, Khan J, Raisuddin S, Parvez S. 2016. Multi-organ toxicological impact of fungicide propiconazole onbiochemical and histological profile of freshwater fish Channa punctata Bloch. Ecological Indicators 63:359–365. DOI: 10.1016/j.ecolind.2015.11.052.
  • Tauchnitz N, Kurzius F, Rupp H, Schmidt G, Hauser B, Schrödter M, Meer R. 2020. Assessment of pesticide inputs into surface waters by agricultural and urban sources - A case study in the Querne/Weida catchment, central Germany. Environmental Pollution 267:115186. DOI: 10.1016/j.envpol.2020.115186.
  • Toni C, Ferreira D, Kreutz LC, Loro VL, Barcellos LJG. 2011a. Assessment of oxidative stress and metabolic changes in common carp (Cyprinus carpio) acutely exposed to different concentrations of the fungicide tebuconazole. Chemosphere 83:579–584. DOI: 10.1016/j.chemosphere.2010.12.022.
  • Toni C, Loro VL, Santi A, De Menezes CC, Cattaneo R, Clasen BE, Zanella R. 2011b. Exposure to tebuconazol in rice field and laboratory conditions induces oxidative stress in carp (Cyprinus carpio). Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 153:128–132. DOI: 10.1016/j.cbpc.2010.09.008.
  • Vani G, Veeraiah K, Kumar MV, Parveen S, Rao DP. 2020. Biochemical changes induced by cartap hydrochloride (50% S.P.), carbamate insecticide in freshwater fish Cirrhinus mrigala (Hamilton, 1822). Nature Environment and Pollution Technology 19:1821–1828. DOI: 10.46488/NEPT.2020.v19i05.005.
  • Wolf JC, Wheeler JR. 2018. A critical review of histopathological findings associated with endocrine and non-endocrine hepatic toxicity in fish models. Aquatic Toxicology 197:60–78. DOI: 10.1016/j.aquatox.2018.01.013.
  • Yadavrao SW. 2017. Confidor and Bavistin induced effects on total glycogen content in liver and gonads of snakeheaded fish, Channa gachua. Journal of Pharmaceutical Innovation 6:41–43.
  • Youness M, Sancelme M, Combourieu B, Besse-Hoggan P. 2018. Identification of new metabolic pathways in the enantioselective fungicide tebuconazole biodegradation by Bacillus sp. 3B6. Journal of Hazardous Materials 351:160–168. DOI: 10.1016/j.jhazmat.2018.02.048.
  • Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A, Payraudeau S, Rasmussen JJ, Rohr J, Scharmüller A, Smalling K. 2019. Fungicides: An overlooked pesticide class? Environmental Science & Technology 53:3347–3365. DOI: 10.1021/acs.est.8b04392.