Acute effects on hepatic biomarkers in the freshwater native fish Aequidens metae exposed to polycyclic aromatic hydrocarbons

Corredor-Santamaría, W.; Calderón-Delgado, I.C.; Arbeli, Z.; Navas, J.M.; Velasco-Santamaría, Y.M.

doi:10.22034/gjesm.2023.01.01

Document Type : ORIGINAL RESEARCH ARTICLE

Authors

¹ Grupo de Investigación en Biotecnología y Toxicología Acuática y Ambiental - BioTox, Escuela de Ciencias Animales, Facultad de Ciencias Agropecuarias y Recursos Naturales, Universidad de los Llanos, Km 12 vía Puerto López, vereda Barcelona, Villavicencio, Colombia

² Unidad de Saneamiento y Biotecnología Ambiental, Departamento de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana, Cra. 7 N. 43-82, Bogotá, Colombia

³ Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), CSIC. Ctra. De la Coruña Km 7.5, E-28040, Madrid, Spain

https://doi.org/10.22034/gjesm.2023.01.01

Abstract

BACKGROUND AND OBJECTIVES: Polycyclic aromatic hydrocarbons are present in all environmental matrices. Polycyclic aromatic hydrocarbons-rich wastewater from the oil industry is discharged into natural water bodies. Detritivorous fish shown the effects of pollutants in water. Biomarkers of effect make it possible to demonstrate exposure to xenobiotics such as polycyclic aromatic hydrocarbons. The aim of the present study was to evaluate the hepatic and erythrocyte response in Aequidens metae , a detritivorous fish, exposed to polycyclic aromatic hydrocarbons in terms of morphological, biochemical, and genotoxic changes.
METHODS: Juveniles of Aequidens metaewere exposed to 50 microgram per gram body weight of beta-naphthoflavone, 100 microgram per gram of naphthalene, 50 microgram per gram of phenanthrene and 10 microgram per gram of benzo[a]pyrene, for 72 hours. Water quality variables, total protein content, 7-ethoxyresorufin-O-deethylase activity, liver histopathological changes and genotoxic alterations in peripheral blood were measured during the assay.
FINDING:In polycyclic aromatic hydrocarbons-exposed fish, analysis of liver tissue revealed parenchymal lesions and changes in the number and shape of hepatocyte nuclei. On the other hand, only fish exposed to benzo[a]pyrene shown significant increase in the 7-ethoxyresorufin-O-deethylase activity compared to solvent control. In peripheral blood erythrocytes, increased presence of nuclear abnormalities was higher in fish exposed to phenanthrene, followed by benzo[a]pyrene, beta-naphthoflavone, and naphthalene.
CONCLUSIONS: It is concluded that Aequidens metae is a suitable bioindicator for polycyclic aromatic hydrocarbons monitoring in aquatic ecosystems. Phenanthrene reveals for the first time a greater genotoxic effect than benzo[a]pyrene at sublethal concentrations. Juveniles ofAequidens metae exposed to concentrations of polycyclic aromatic hydrocarbons close to those found in the environment showed health-compromising damage.

Graphical Abstract

Highlights

At sublethal doses phenanthrene, benzo[a]pyrene and naphthalene induce nuclear abnormalities in peripheral blood of juvenile Aequidens metae;

Benzo[a]pyrene and B-naphthoflavone induce at realistic environmental concentrations EROD activity in liver of metae;

Intraperitoneal exposure to BaP, phenanthrene and naphthalene induces reversible moderate alterations in liver of metae.

Keywords

Main Subjects

Environmental health and ecotoxicology

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References

Abalaka, S.E.; Fatihu, M.Y.; Ibrahim, N.D.G.; Ambali, S.F., (2015). Gills and skin histopathological evaluation in African sharptooth catfish, Clarias gariepinus exposed to ethanol extract of Adenium obesum stem bark. Egypt. J. Aquat. Res., 41(1): 119–127 (9 pages).

Al-Ghais, S.M., (2013). Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar. Pollut. Bull., 74(1): 183–186 (4 pages).

Aly, W.; Abouelfadl, K.Y., (2020). Impact of low-level water pollution on some biological aspects of redbelly tilapia (Coptodon zillii) in River Nile, Egypt. Egypt. J. Aquat. Res., 46(3): 273–279 (7 pages).

Al-Sabti, K.; Metcalfe, C.D., (1995). Fish micronuclei for assessing genotoxicity in water. Mutat. Res. Genet. Toxicol., 343(2-3): 121–135 (15 pages).

Amutha, C.; Subramanian, P., (2010). Effect of temperature, salinity, pH and naphthalene on ethoxyresorufin- O -deethylase activity of Oreochromis mossambicus. Toxicol. Environ. Chem., 92(1), 127–135 (9 pages).

Araújo, F.G.; Morado, C.N.; Parente, T.T.E.; Paumgartten, F.J.R.; Gomes, I.D., (2017). Biomarkers and bioindicators of the environmental condition using a fish species (Pimelodus maculatus Lacepède, 1803) in a tropical reservoir in Southeastern Brazil. Braz. J. Biol., 78(2): 351–359 (9 pages).

Bhagat, J.; Sarkar, A.; Ingole, B.S., (2016). DNA Damage and Oxidative Stress in Marine Gastropod Morula granulata Exposed to Phenanthrene. Water Air Soil Pollut., 227(4): 114 (12 pages).

Beltrán, J.D.; Vargas, C.A., (2014). Hydrocarbon Production Scenarios in Colombia. Review of Field Sizes, Hydrocarbon Reserves and Expectations of Conventional and Unconventional Resources. Earth Sci. Res. J., 18(1): 77-83 (7 pages).

Briaudeau, T.; Alves Dos Santos, L.A.; Zorita, I.; Izagirre, U.; Marigómez, I., (2021). Biological responses and toxicopathic effects elicited in Solea senegalensis juveniles by waterborne exposure to benzo[a]pyrene. Mar. Environ. Res., 170: 105351 (12 pages).

Brzuzan, P.; Jurczyk, Ł.; Woźny, M.; Góra, M.; Łuczyński, M.K.; Kuźmiński, H.; Nitek, W., (2006). Molecular geometry, cyp1a gene induction and clastogenic activity of cyclopenta[c]phenanthrene in rainbow trout. Polycyclic Aromat. Compd., 26(5): 345–365 (22 pages).

Burke, M.D.; Mayer, R.T., (1974). Ethoxyresoruﬁn: direct ﬂuorimetric assay of a microsomal O-dealkylation which is preferentially inducible by 3methylcholanthrene. Drug Metab. Dispos., 2: 583–588 (6 pages).

Carrasco, K.; Tilbury, K.L.; Myers, M.S., (1990). Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can. J. Fish. Aquat. Sci., 47(11): 2123–2136 (13 pages).

Çavaş, T.; Ergene-Gözükara, S., (2005). Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat. Toxicol., 74 (3): 264–271 (7 pages).

Corredor-Santamaría, W.; Gómez-Serrano, M.; Velasco-Santamaría, Y.M., (2016). Using Genotoxic and Haematological Biomarkers as an Evidence of Environmental contamination in the Ocoa River native fish, Villavicencio—Meta, Colombia. Springerplus. 5(1); (10 pages).

Corredor-Santamaría, W.; Mora-Solarte, D.A.; Arbeli, Z.; Navas, J.M.; Velasco-Santamaría, Y.M., (2021). Liver biomarkers response of the neotropical fish Aequidens metae to environmental stressors associated with the oil industry. Heliyon, 7(7): e07458 (8 pages).

Corredor-Santamaría, W.; Torres-Tabares, A.; Velasco-Santamaría, Y.M., (2019). Biochemical and histological alterations in Aequidens metae (Pisces, Cichlidae) and Astyanax gr. bimaculatus (Pisces, Characidae) as indicators of river pollution. Sci. Total Environ., 692: 1234–1241 (7 pages).

Cousin, X.; Cachot, J., (2014). PAH and fish—exposure monitoring and adverse effects—from molecular to individual level. Environ. Sci. Pollut. Res., 21(24): 13685–13688 (4 pages).

Dane, H.; Şişman, T., (2014). Histopathological changes in gill and liver of Capoeta capoeta living in the Karasu River, Erzurum. Environ. Toxicol., 30(8): 904–917 (13 pages).

De, S.; Maiti, S.; Hazra, T.; Debsarkar, A.; Dutta, A., (2016). Leachate characterization and identification of dominant pollutants using leachate pollution index for an uncontrolled landfill site. Global J. Environ. Sci. Manage., 2(2): 177-186 (10 pages).

Esmaeilbeigi, M.; Kalbassi, M.R.; Seyedi, J.; Tayemeh, M.B.; Moghaddam, J.A., (2021). Intra and extracellular effects of benzo [α] pyrene on liver, gill and blood of Caspian White fish (Rutilus frissi kutum): Cyto-genotoxicity and histopathology approach. Mar. Pollut. Bull., 163: 111942 (9 pages).

Fanali, L.Z.; De Oliveira, C.; Sturve, J., (2021). Enzymatic, morphological, and genotoxic effects of benzo[a]pyrene in rainbow trout (Oncorhynchus mykiss). Environ. Sci. Pollut. Res., 28(38): 53926–53935 (10 pages).

Gao, K.; Tian, J.; Wu, Y.; Mei, P.; Zhang, Z.; Jönsson, M.; Brandt, I., (2021). Induction of cytochrome P4501 genes by various inducers in rainbow trout (Oncorhynchus mykiss). J. Coastal Res., 37(1): 143–148 (6 pages).

Gan, N.; Martin, L.; Xu, W., (2021). Impact of Polycyclic Aromatic Hydrocarbon Accumulation on Oyster Health. Front. Physiol., 12 (21 pages).

Gerger, C.J.; Weber, L.P., (2015). Comparison of the acute effects of benzo-a-pyrene on adult zebrafish (Danio rerio) cardiorespiratory function following intraperitoneal injection versus aqueous exposure. Aquat. Toxicol., 165: 19–30 (12 pages).

Grisolia, C.K., (2002). A comparison between mouse and fish micronucleus test using cyclophosphamide, mitomycin C and various pesticides. Mutat. Res. - Genet. Toxicol. Environ. Mutagen. 518: 145–150 (6 pages).

Gu, X.; Manautou, J.E., (2012). Molecular mechanisms underlying chemical liver injury. Expert Rev. Mol. Med., 14: e4 (21 pages).

Honda, M.; Suzuki, N., (2020). Toxicities of Polycyclic Aromatic Hydrocarbons for Aquatic Animals. Int. J. Environ. Res. Public Health. 17(4): 1363 (23 pages).

Javed, M.; Usmani, N., (2019). An Overview of the Adverse Effects of Heavy Metal Contamination on Fish Health. Proc. Natl. Acad. Sci. India B - Biol. Sci., 89(2): 389–403 (15 pages).

Jönsson, M.E.; Gao, K.; Olsson, J.A.; Goldstone, J.V.; Brandt, I., (2010). Induction patterns of new CYP1 genes in environmentally exposed rainbow trout. Aquat. Toxicol., 98(4): 311–321 (11 pages).

Karami, A.; Christianus, A.; Ishak, Z.; Syed, M.A.; Courtenay, S.C., (2011). The effects of intramuscular and intraperitoneal injections of benzo[a]pyrene on selected biomarkers in Clarias gariepinus. Ecotoxicol. Environ. Saf., 74(6): 1558–1566 (9 pages).

Karbassi, A.R.; Heidari, M., (2015). An investigation on role of salinity, pH and DO on heavy metals elimination throughout estuarial mixture. Global J. Environ. Sci. Manage., 1(1): 41-46 (6 pages).

Khaniyan, M.; Salamat, N.; Safahieh, A.; Movahedinia, A., (2016). Detection of benzo[a]pyrene-induced immunotoxicity in orange spotted grouper (Epinephelus coioides). Environ. Toxicol., 31(3): 329–338 (10 pages).

Kostić, J.; Kolarević, S.; Kračun-Kolarević, M.; Aborgiba, M.; Gačić, Z.; Paunović, 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., 601-602: 1670–1681 (12 pages).

Mai, Y.; Peng, S.; Li, H.; Gao, Y.; Lai, Z., (2021). NOD-like receptor signaling pathway activation: A potential mechanism underlying negative effects of benzo(α)pyrene on zebrafish. Comp. Biochem. Physiol. Part - C: Toxicol. Pharmacol., 240: 108935 (14 pages).

Matsumoto, S.T.; Mantovani, M.S.; Malaguttii, M.I.A.; Dias, A.L.; Fonseca, I.C.; Marin-Morales, M.A., (2006). Genotoxicity and mutagenicity of water contaminated with tannery effluents, as evaluated by the micronucleus test and comet assay using the fish Oreochromis niloticus and chromosome aberrations in onion root-tips. Genet. Mol. Biol., 29(1): 148–158 (11 pages).

McGrath, J.A.; Joshua, N.; Bess, A.S.; Parkerton, T.F. (2019). Review of Polycyclic Aromatic Hydrocarbons (PAHs) Sediment Quality Guidelines for the Protection of Benthic Life. Integr. Environ. Assess. Manage., 15(4): 505–518 (14 pages).

Meier, S.; Karlsen, Ø.; Le Goff, J.; Sørensen, L.; Sørhus, E.; Pampanin, D.M.; Donald, C.E.; Fjelldal, P. G.; Dunaevskaya, E.; Romano, M.; Caliani, I.; Casini, S.; Bogevik, A.S.; Olsvik, P.A.; Myers, M.; Grøsvik, B.E., (2020). DNA damage and health effects in juvenile haddock (Melanogrammus aeglefinus) exposed to PAHs associated with oil-polluted sediment or produced water. PLOS ONE, 15(10), e0240307 (34 pages).

Mora-Solarte, D.A.; Calderón-Delgado, I.C.; Velasco-Santamaría, Y.M. (2020). Biochemical responses and proximate analysis of Piaractus brachypomus (Pisces: Characidae) exposed to phenanthrene. Comp. Biochem. Physiol. Part - C: Toxicol. Pharmacol., 228, 108649 (7 pages).

Myers, M.S.; Anulacion, B.F.; French, B.L.; Reichert, W.L.; Laetz, C.A.; Buzitis, J.; Olson, O.P.; Sol, S.; Collier, T.K., (2008). Improved flatfish health following remediation of a PAH-contaminated site in Eagle Harbor, Washington. Aquat. Toxicol., 88(4): 277–288 (12 pages).

Noman, M.A.; Feng, W.; Zhu, G.; Hossain, M.B.; Chen, Y.; Zhang, H.; Sun, J., (2022). Bioaccumulation and potential human health risks of metals in commercially important fishes and shellfishes from Hangzhou Bay, China. Sci. Rep., 12(1): 4634 (15 pages).

Olayinka, O.O.; Adewusi, A.A.; Olujimi, O.O.; Aladesida, A.A. (2019). Polycyclic aromatic hydrocarbons in sediment and health risk of fish, crab and shrimp around Atlas Cove, Nigeria. J. Health Pollut., 9(24), (21 pages).

Oliva, M.; Gravato, C.; Guilhermino, L.; Galindo-Riaño, M.D.; Perales, J A., (2014). EROD activity and cytochrome P4501A induction in liver and gills of Senegal sole Solea senegalensis from a polluted Huelva Estuary (SW Spain). Comp. Biochem. Physiol. Part - C: Toxicol. Pharmacol., 166: 134–144 (11 pages).

Oliveira, H.H.P.; Babin, M.; Garcia J.R.E.; Filipak Neto, F.; Randi, M.A.F.; Oliveira, C.A., (2013). Complex metabolic interactions between benzo(a)pyrene and tributyltin in presence of dichlorodiphenyltrichloroethane in South American catfish Rhamdia quelen. Ecotoxicol. Environ. Saf., 96: 67–74 (8 pages).

Oliveira, M.; Pacheco, M.; Santos, M.A., (2007). Cytochrome P4501A, genotoxic and stress responses in golden grey mullet (Liza aurata) following short-term exposure to phenanthrene. Chemosphere. 66(7): 1284–1291 (8 pages).

Ossai, I.C.; Ahmed, A.; Hassan, A.; Hamid, F.S., (2020). Remediation of soil and water contaminated with petroleum hydrocarbon: A review. Environ. Technol. Innov., 17: 100526 (42 pages).

Pulster, E.L.; Main, K.; Wetzel, D.; Murawski, S. (2017). Species-specific metabolism of naphthalene and phenanthrene in 3 species of marine teleosts exposed to Deepwater Horizon crude oil. Environ. Toxicol, Chem., 36(11): 3168–3176 (9 pages).

Reddam, A.; Mager, E.M.; Grosell, M.; McDonald, M.D., (2017). The impact of acute PAH exposure on the toadfish glucocorticoid stress response. Aquat. Toxicol., 192: 89–96 (8 pages).

Regnault, C.; Worms, I.A.; Oger-Desfeux, C.; MelodeLima, C.; Veyrenc, S.; Bayle, M.L.; Combourieu, B.; Bonin, A.; Renaud, J.; Raveton, M.; Reynaud, S., (2014). Impaired liver function in Xenopus tropicalis exposed to benzo[a]pyrene: transcriptomic and metabolic evidence. BMC Genom., 15(1): 666 (16 pages).

Reis-Henriques, M.A.; Ferreira, M.; Coimbra, A.M.; D'Silva, C.; Costa, J.; Shailaja, M.S., (2009). Phenanthrene and nitrite effects on juvenile sea bass, Dicentrarchus labrax, using hepatic biotransformation enzymes, biliary fluorescence, and micronuclei as biomarkers. Health Environ. Re. Online. 35(1): 29-40 (12 pages).

Rodrigues, A.C.F.; de Oliveira Moneró, T.; Frighetto, R.T.S.; de Almeida, E.A., (2014). E2 potentializes benzo(a)pyrene-induced hepatic cytochrome P450 enzyme activities in Nile tilapia at high concentrations. Environ. Sci. Pollut. Res., 22(22): 17367–17374 (8 pages).

Samanta, P.; Im, H.; Na, J.; Jung, J., (2018). Ecological risk assessment of a contaminated stream using multi-level integrated biomarker response in Carassius auratus. Environ. Pollut., 233: 429–438 (10 pages).

Santos, C.; de Oliveira, M.T.; Cólus, I.M. de S.; Sofia, S.H.; Martinez, C.B. dos R., (2018). Expression of cyp1a induced by benzo(A)pyrene and related biochemical and genotoxic biomarkers in the neotropical freshwater fish Prochilodus lineatus. Environ. Toxicol. Pharmacol., 61: 30–7 (8 pages).

Shirmohammadi, M.; Salamat, N.; Taghi Ronagh, M.; Movahedinia, A.; Hamidian, G., (2017). Effect of Phenanthrene on the Tissue Structure of Liver and Aminotransferase Enzymes in Yellowfin Seabream (Acanthopagrus latus). Iran. J. Toxicol., 11(4): 33–41 (13 pages).

Snyder, S.M.; Pulster, E.L.; Wetzel, D.L.; Murawski, S.A., (2015). PAH Exposure in Gulf of Mexico Demersal Fishes, Post- Deepwater Horizon. Environ. Sci. Technol., 49(14): 8786–8795 (10 pages).

Torreiro-Melo, A.G.A.G.; Silva, J.S.; Bianchini, A.; Zanardi-Lamardo, E.; Carvalho, P.S.M. de., (2015). Bioconcentration of phenanthrene and metabolites in bile and behavioral alterations in the tropical estuarine guppy Poecilia vivipara. Chemosphere., 132: 17–23 (7 pages).

Valdehita, A.; Fernández-Cruz, M.L.; Torrent, F.; Sericano, J.L.; Navas, J.M., (2012). Differences in the induction of cyp1A and related genes in cultured rainbow trout Oncorhynchus mykiss. Additional considerations for the use of EROD activity as a biomarker. J. Fish Biol., 81(1): 270–287 (18 pages).

Velasco-Santamaría, Y.M.; Corredor-Santamaría, W.; Torres-Tabares, A., (2019). Environmental Pollution by Hydrocarbons in Colombia and Its Impact on the Health of Aquatic Ecosystems. In: Gómez L.M. (eds) Pollution of Water Bodies in Latin America. 229–254 (26 pages). Springer Nature Switzerland AG (25 pages).

Velma, V.; Tchounwou, P.B., (2010). Chromium-induced biochemical, genotoxic and histopathologic effects in liver and kidney of goldfish, Carassius auratus. Mutat. Res. - Genet. Toxicol. Environ. Mutagen., 698(1–2): 43–51 (9 pages).

Wang, H.; Xia, X.; Wang, Z.; Liu, R.; Muir, D.C.G.; Wang, W.X., (2021). Contribution of Dietary Uptake to PAH Bioaccumulation in a Simplified Pelagic Food Chain: Modeling the Influences of Continuous vs Intermittent Feeding in Zooplankton and Fish. Environ. Sci. Technol., 55(3): 1930–1940 (11 pages).

Wincent, E.; Le Bihanic, F.; Dreij, K., (2016). Induction and inhibition of human cytochrome P4501 by oxygenated polycyclic aromatic hydrocarbons. Toxicol. Res., 5(3): 788–799 (12 pages).

Wolf, J.C., (2013). Alternative Animal Models. In: W. M. Haschek, C. G. Rousseaux, & M. A. Wallig (Eds.), Haschek and Rousseaux’s Handbook of Toxicologic Pathology. 477–518 (42 pages).

Wolf, J.C.; Wheeler, J.R., (2018). A critical review of histopathological findings associated with endocrine and non-endocrine hepatic toxicity in fish models. Aquat. Toxicol, 197: 60–78 (19 pages).

Xu, W.; Li, Y.; Wu, Q.; Wang, S.; Zheng, H.; Liu, W., (2009). Effects of phenanthrene on hepatic enzymatic activities in tilapia (Oreochromis niloticus ♀ × O. aureus ♂). J. Environ. Sci., 21(6): 854–857 (4 pages).

Yasui, M.; Kamoshita, N.; Nishimura, T.; Honma, M., (2015). Mechanism of induction of binucleated cells by multiwalled carbon nanotubes as revealed by live-cell imaging analysis. Genes Environ., 37(1): 6 (6 pages).

Yu, Z.; Lin, Q.; Gu, Y.; Du, F.; Wang, X.; Shi, F.; Ke, C.; Xiang, M.; Yu, Y. (2019). Bioaccumulation of polycyclic aromatic hydrocarbons (PAHs) in wild marine fish from the coastal waters of the northern South China Sea: Risk assessment for human health. Ecotoxicol. Environ. Saf., 180: 742–748 (7 pages).

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