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The applied indicators of water quality may underestimate the risk of chemical exposure to human population in reservoirs utilized for human supply—Southern Brazil

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The knowledge concerning associations between chronic chemical exposure and many disorders with complex etiology involving gene–environment interactions is increasing, and new methods must be developed to improve water quality monitoring. The complexity of chemical mixtures in polluted aquatic environments makes the evaluation of toxic potential in those sites difficult, but the use of biomarkers and bioindicators has been recognized as a reliable tool to assess risk of exposure to biota and also the human population. In order to evaluate the use of fish and biomarkers to assess toxic potential and bioavailability of chemicals in human-related hydric resources, an in situ experiment was accomplished in two water reservoirs designated for human supply, which were previously evaluated by the local environmental regulatory agency through a set of physical, chemical, and classical biological parameters. Molecular, biochemical, and morphological biomarkers were performed in caged Oreochromis niloticus kept for 6 months in the studied reservoirs to assess potentially useful biomarkers to evaluate the quality of water for human supply. Chemical analysis of toxic metals in liver and muscle and polycyclic aromatic hydrocarbons (PAHs) in bile was considered to assess the bioavailability of pollutants and highlight human activity impact. The reservoir previously classified by a governmental agency as less impacted presented more risk of exposure to biota. These results were supported by chemical analysis, vitellogenin expression, histopathological findings (gonads, liver, and gills), as well as indicators of neurotoxic effects and oxidative stress in liver. The inclusion of some biomarkers as parameters in regulatory monitoring programs in reservoirs designated for human supply is strongly suggested to evaluate the risks of exposure to the human population. Thus, a revision of the traditional biological and physicochemical analysis utilized to establish the conditions of water quality is necessary.

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  1. Abdel-moneim AM, Al-kahtani MA, Elmenshawy OM (2012) Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere 88(8):1028–1035. doi:10.1016/j.chemosphere.2012.04.001

  2. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

  3. Almroth BC, Sturvea J, Eiríkur Stephensenb E, Tor Fredrik Holthc TF, Förlina L (2008) Protein carbonyls and antioxidant defenses in corkwing wrasse (Symphodus melops) from a heavy metal polluted and a PAH polluted site. Mar Environ Res 66(2):271–277. doi:10.1016/j.marenvres.2008.04.002

  4. ANA (2012) Agência Nacional das Águas (Brasil). Surface fresh water quality in Brazil, outlook (2012), Executive summary/ Agência Nacional de Águas. ANA, Brasília, 64 p. ISBN: 978-85-8210-006-6

  5. Atli G, Canli M (2010) Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Saf 73(8):1884–1889. doi:10.1016/j.ecoenv.2010.09.005

  6. Barakat AO, Mostafa A, Wade TL, Sweet ST, El Sayed NB (2011) Distribution and characteristics of PAHs in sediments from the Mediterranean coastal environment of Egypt. Mar Pollut Bull 62(9):1969–1978. doi:10.1016/j.marpolbul.2011.06.024

  7. Barbee GC, Barich J, Duncan B (2008) In situ biomonitoring of PAH-contaminated sediments using juvenile coho salmon (Oncorhynchus kisutch). Ecotoxicol Environ Saf 71(2):454–464. doi:10.1016/j.ecoenv.2008.01.001

  8. Barber LB, Brown GK, Nettesheim TG, Murphy EW, Barteli SE, Schoenfuss HL (2011) Effects of biologically-active chemical mixtures on fish in a wastewater-impacted urban stream. Sci Total Environ 409:4720–4728. doi:10.1016/j.scitotenv.2011.06.039

  9. 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(1):25–34. doi:10.1046/j.1365-2761.1999.00134.x

  10. Besse JP, Geffard O, Coquery M (2012) Relevance and applicability of active biomonitoring in continental waters under the water framework directive. Trends Anal Chem 36:113–127. doi:10.1016/j.trac.2012.04.004

  11. Blanco S, Bécares E (2010) Are biotic indices sensitive to river toxicants? A comparison of metrics based on diatoms and macro-invertebrates. Chemosphere 79(1):18–25. doi:10.1016/j.chemosphere.2010.01.059

  12. Boelsterli URSA (2007) Mechanistic toxicology, 2nd edn, The molecular basis of how chemicals disrupt biological targets. CRC Press Taylor-Francis, London, 416 p

  13. Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58. doi:10.1007/s10886-009-9730-5

  14. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  15. Bretaud S, Toutant J, Saglio P (2000) Effects of carbofuran, diuron, and nicosulfuron on acetylcholinesterase activity in goldfish (Carassius auratus). Ecotoxicol Environ Saf 47:117–124

  16. Cavalheiro de Menezes C, Loro VL, da Fonseca Milene Braga MB, Cattaneo R, Pretto A, Miron DS, Adriana Santi A (2011) Oxidative parameters of Rhamdia quelen in response to commercial herbicide containing clomazone and recovery pattern. Pestic Biochem Physiol 100(2):145–150. doi:10.1016/j.pestbp.2011.03.002

  17. Cazenave J, Bacchetta C, Parma MJ, Scarabotti PA, Wunderlin DA (2009) Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the water quality of Salado River basin (Santa Fe, Argentina). Environ Pollut 157(11):3025–3033. doi:10.1016/j.envpol.2009.05.055

  18. Costa PM, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, Costa MH (2011) Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish. Mar Pollut Bull 62(1):55–65. doi:10.1016/j.marpolbul.2010.09.009

  19. Costa-Pierce BA (2003) Rapid evolution of an established feral tilapia (Oreochromis spp.): the need to incorporate invasion science into regulatory structures. Biological Invasions Magazine 5:71–84

  20. Darbre PD (2015) How could endocrine disrupters affect human health? Endocrine Disruption and Human Health, 27–45

  21. Ellman GL, Courtney D, Andres V Jr, Feathersthone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–96

  22. FAO (2007) Fisheries and Aquaculture Department. Species fact sheets Oreochromis niloticus (Linnaeus, 1758). Available in: Accessed in: November 2015

  23. Fernandes D, Porte C (2013) Hydroxylated PAHs alter the synthesis of androgens and estrogens in subcellular fractions of carp gonads. Sci Total Environ 447:152–159. doi:10.1016/j.scitotenv.2012.12.068

  24. FishBase (2007) Oreochromis niloticus niloticus Nile tilapia: summary. Available in: Accessed in: November 2015

  25. Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22(4):241–253. doi:10.1111/j.1439-0426.2006.00805.x

  26. Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20(1):37–45

  27. Hanson H, Larson M (2008) Implications of extreme waves and water levels in the southern Baltic Sea. J Hydraul Res 46:292–302. doi:10.1080/00221686.2008.9521962

  28. He X, Nie X, Wang Z, Cheng Z, Li K, Li G, Hung Wong M, Liang X, Tsui MT (2011) Assessment of typical pollutants in waterborne by combining active biomonitoring and integrated biomarkers response. Chemosphere 84(10):1422–1431. doi:10.1016/j.chemosphere.2011.04.054

  29. IAP (2009) Instituto Ambiental do Paraná. Qualidade das Águas – Reservatórios do Estado do Paraná no período de 2005 a 2008. 120p. Ed. Fundamento, Brasil. (in Portuguese). Available in:

  30. Jiang Z-Y, Woollard ACS, Wolff SP (1991) Lipid hydroperoxides measurement by oxidation of Fe2+ in the presence of xylenol orange. comparison with the TBA assay and an iodometric method. Lipids 26:853–856

  31. Keen JH, Habig WH, Jakoby WB (1976) Mechanism for several activities of the gluthatione S-transferases. J Biol Chem 251:6183–6188

  32. Kummer V, Masková J, Zralý Z, Neca J, Simecková P, Vondrácek J, Machala M (2008) Estrogenic activity of environmental polycyclic aromatic hydrocarbons in uterus of immature Wistar rats. Toxicol Lett 180(3):212–221. doi:10.1016/j.toxlet.2008.06.862

  33. Leino RL, Jensen KM, Ankley GT (2005) Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephales promelas). Environ Toxicol Pharmacol 19(1):85–98. doi:10.1016/j.etap.2004.05.010

  34. Levine RL, Williams JA, Stadtman EP, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

  35. Li Z, Zhang H, Gibson M, Liu P (2012) An evaluation of the combined effects of phenolic endocrine disruptors on vitellogenin induction in goldfish Carassius auratus. Ecotoxicology 21(7):1919–1927. doi:10.1007/s10646-012-0925-0

  36. Louiz I, Ben-Attia M, Ben-Hassine OK (2009) Gonadosomatic index and gonad histopathology of Gobius niger (Gobiidea, Teleost) from Bizerta lagoon (Tunisia): evidence of reproduction disturbance. Fish Res 100(3):266–273. doi:10.1016/j.fishres.2009.08.009

  37. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK (2013) Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS ONE 8:1–18. doi:10.1371/journal.pone.0055387

  38. Matozzo V, Gagné F, Marin MG, Ricciardi F, Blaise C (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34(4):531–545. doi:10.1016/j.envint.2007.09.008

  39. Moura Costa DDM, Neto FF, Costa MDM, Morais RN, Garcia JRE, Esquivel BM, Ribeiro C a O (2010) Vitellogenesis and other physiological responses induced by 17-β-estradiol in males of freshwater fish Rhamdia quelen. Comp Biochem Physiol, Part C: Toxicol Pharmacol 151(2):248–257. doi:10.1016/j.cbpc.2009.11.002

  40. Nogueira P, Pacheco M, Pereira ML, Mendo S, Rotchell JM (2010) Anchoring novel molecular biomarker responses to traditional responses in fish exposed to environmental contamination. Environ Pollut 158:1783–1790

  41. Oliveira Ribeiro CA, Narciso MF (2014) Histopatological Markers in Fish Health Assessment. In: Almeida EA, Oliveira Ribeiro CA (eds) Pollution and fish health in tropical exosystems. CRC Press, Boca Raton, pp 206–242

  42. Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem Biol Interact 174(3):183–192. doi:10.1016/j.cbi.2008.05.014

  43. Parveza S, Raisuddinb S (2005) Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environ Toxicol Pharmacol 20(1):112–117. doi:10.1016/j.etap.2004.11.002

  44. Quinlan GJ, Gutteridge JMC (2000) Carbonyl assay for oxidative damage to proteins. In: Taniguchi N, Gutteridge JMC (eds) Experimental protocols for reactive oxygen and nitrogen species. Oxford University, New York, pp 257–258

  45. Rabitto IS, Costa JRMA, Silva de Assis HC, Pelletier E, Akaishi FM, Anjos A, Randi MAF, Ribeiro CAO (2005) Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: histopathological and biochemical findings. Ecotoxicol Environ Saf 60:147–156

  46. Rabitto IS, Bastos WR, Almeida R, Anjos A, Holanda IBB, Galvao RCF, Neto FF, Menezes ML, Santos CAM, Ribeiro CAO, Moraes CA (2011) Mercury and DDT exposure risk to fish-eating human populations in Amazon. Environ Int 37:56–65. doi:10.1016/j.envint.2010.07.001

  47. Rodrigues SR, Caldeira C, Castro BB, Gonçalves F, Nunes B, Antunes SC (2011) Cholinesterase (ChE) inhibition in pumpkinseed (Lepomis gibbosus) as environmental biomarker: ChE characterization and potential neurotoxic effects of xenobiotics. Pestic Biochem Physiol 99(2):181–188. doi:10.1016/j.pestbp.2010.12.002

  48. Sanchez W, Porcher JM (2009) Fish biomarkers for environmental monitoring within the water framework directive of the European Union. TrAC Trends Anal Chem 28(2):150–158. doi:10.1016/j.trac.2008.10.012

  49. Sanchez W, Palluel O, Lagadic L, Ait-Aissa S, Porcher JM (2006) Biochemical effects of nonylphenol polyethoxylate adjuvant, Diquat herbicide and their mixture on the three-spined stickleback (Gasterosteus aculeatus L.). Mar Environ Res 62:S29–S33. doi:10.1016/j.marenvres.2006.04.028

  50. Scholz S, Mayer I (2008) Molecular biomarkers of endocrine disruption in small model fish. Mol Cell Endocrinol 293(1–2):57–70. doi:10.1016/j.mce.2008.06.008

  51. Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25(1):192–205

  52. Silva JPA, Muelbert AE, Oliveira EC, Fávaro LF (2010) Reproductive tactics used by the Lambari Astyanax aff. fasciatus in three water supply reservoirs in the same geographic region of the upper Iguaçu River. Neotropical Ichthyology 8(4):885–892

  53. Silversand C, Hyllner SJ, Haux C (1993) Isolation, immunochemical detection, and observations of the instability of vitellogenin from four teleosts. J Exp Zool 267:587–597. doi:10.1002/jez.1402670606

  54. Taxvig C, Hadrup N, Boberg J, Axelstad M, Bossi R, Bonefeld-Jorgensen EC, Vinggaard AM (2013) In vitro-in vivo correlations for endocrine activity of a mixture of currently used pesticides. Toxicol Appl Pharmacol 272:757–766. doi:10.1016/j.taap.2013.07.028

  55. Thompson KC, Wadhia K, Loibner A (2005) Environmental toxicity testing. 1st Ed. Blackwell Publishing Ltd. 83–85

  56. Van Der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149. doi:10.1016/S1382-6689(02)00126-6

  57. Van Dyk JC, Cochrane MJ, Wagenaar GM (2012) Liver histopathology of the sharp tooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere 87(4):301–311. doi:10.1016/j.chemosphere.2011.12.002

  58. Venancio LPR, Domingos CRB (2014) Effect of pollutants on condition index. In: Almeida EA, Oliveira Ribeiro CA (eds) Pollution and fish health in tropical ecosystems. CRC Press, Boca Raton, pp 338–349

  59. Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606(2):135–150

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This work was supported by the National Council of Science and Technology—CNPq, Coordination for the Improvement of Higher Educational Personnel—CAPES, and State Agency of Science and Technology of Parana—Araucaria Foundation. The authors thank the Sanitation Company of Parana—SANEPAR for logistic support in the reservoirs and the Center of Electron Microscopy at Federal University of Parana for technical support.

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Correspondence to Ciro Alberto de Oliveira Ribeiro.

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Responsible editor: Philippe Garrigues

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dos Santos, D.R., Yamamoto, F.Y., Filipak Neto, F. et al. The applied indicators of water quality may underestimate the risk of chemical exposure to human population in reservoirs utilized for human supply—Southern Brazil. Environ Sci Pollut Res 23, 9625–9639 (2016).

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  • Biomarkers
  • Transplanted fish
  • Aquatic pollution
  • Water quality
  • Water reservoir