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Genotoxicity Biomarkers in Fish Erythrocytes and Water Quality Parameters

  • Thaís Dalzochio
  • Natália Bordin Andriguetti
  • Leonardo Airton Ressel Simões
  • Günther Gehlen
  • Luciano Basso da Silva
Chapter

Abstract

Ecotoxicological approaches in water quality assessment have become important tools in environmental studies. The analysis of biomarkers in biological organisms collected in situ or exposed to water samples under laboratory conditions provides information on the effects of substances (heavy metals, pesticides, polycyclic aromatic hydrocarbons, and other emerging contaminants). The genotoxicity evaluation carried out, among others, by the micronucleus test in fish erythrocytes, provides information on the potential DNA damage caused by the exposure to a single or a complex mixture of pollutants. Moreover, the combined analysis of genotoxic endpoints to water physicochemical parameters provides more realistic data on the pollution scenario. In Brazil, a number of studies have evidenced the poor water quality of the Sinos River basin – an important water resource located in the Southern region. A case study of this basin is presented in this chapter, where water physicochemical analysis and the micronucleus test in fish erythrocytes were performed. Some water parameters were found above the limits established by the Brazilian legislation. In contrast, no genotoxic effect was evidenced in the fish Cyprinus carpio exposed for 72 h to water samples collected at seven sampling sites distributed along the basin. Nonetheless, the continuous assessment through ecotoxicological approaches is invaluable to environmental diagnosis.

Keywords

Water quality Sinos River Micronucleus test Cyprinus carpio Genotoxicity 

References

  1. Akinboro A, Mohammed K, Rathnasamy S, Muniandy VR (2011) Genotoxicity assessment of water samples from the Sungai Dua river in Pulau Pinang, Malaysia, using the Allium cepa test. Trop Life Sci Res 22:23–35PubMedPubMedCentralGoogle Scholar
  2. Alloway BJ (2013) Heavy metals in soils. Trace metals and metalloids in soils and their bioavailability.. Environ Poll 22. Springer Netherlands, NetherlandsGoogle Scholar
  3. Al-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343(2–3):121–135CrossRefPubMedPubMedCentralGoogle Scholar
  4. APHA – American Public Health Association (2005) Standard methods for the examination of water and wastewater, twenty-first ed. APHA, Washington, D.C., p 1220Google Scholar
  5. Araújo ALS, Guimarães ET, Seriani R (2014) Mutagenesis in Tradescantia pallida as a biomarker of the effects of water polluted with urban effluent. Holos Environ 14(1):97–102CrossRefGoogle Scholar
  6. Ayllón F, Garcia-Vasquez E (2001) Micronuclei and other nuclear lesions as in rainbow trout Oncorhynchus mykiss. Ecotoxicol Environ Safe 49(3):221–225CrossRefGoogle Scholar
  7. Azevedo JS, Braga ES, Assis HCE, Ribeiro CAO (2013) Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying influences of anthropogenic activities. Ecotoxicol Environ Safe 96:220–230CrossRefGoogle Scholar
  8. Batista NJC, Cavalcante AACM, Oliveira MG, Medeiros ECN, Machado JL, Evangelista SR, Dias JF, Santos CEI, Duarte A, Silva FR, Silva J (2016) Genotoxic and mutagenic evaluation of water samples from a river under the influence of diferente anthropogenic activities. Chemosphere 164:134–141CrossRefPubMedPubMedCentralGoogle Scholar
  9. Benvenuti T, Kieling-Rubio MA, Klauck CR, Rodrigues MAS (2015) Evaluation of water quality at the source of streams of the Sinos River Basin, southern Brazil. Braz J Biol 75(S2):S98–S104CrossRefGoogle Scholar
  10. Bergamaschi B, Rodrigues MT, Silva JVS, Kluge M, Luz RB, Fleck JD, Bianchi E, Silva LB, Spilki FR (2015) Moving beyond classical markers of water quality: detection of enteric viruses and genotoxicity in water of the Sinos River. Braz J Biol 75(S2):S63–S67CrossRefGoogle Scholar
  11. Bianchi J, Espindola ELG, Marin-Morales MA (2011) Genotoxicity and mutagenicity of water samples from the Monjolinho River (Brazil) after receiving untreated effluents. Ecotoxicol Environ Safe 74:826–833CrossRefGoogle Scholar
  12. Bianchi E, Goldoni A, Trintinaglia L, Lessing G, Silva CEM, Nascimento CA, Ziulkoski AL, Spilki FR, Silva LB (2015) Evaluation of genotoxicity and cytotoxicity of water samples from the Sinos River Basin, southern Brazil. Braz J Biol 75(S2):S68–S74CrossRefGoogle Scholar
  13. Bianchi E, Lessing G, Brina KR, Angeli L, Andriguetti NB, Peruzzo JRS, Nascimento CA, Spilki FR, Ziulkoski AL, Silva LB (2017) Monitoring the genotoxic and cytotoxic potential and the presence of pesticides and hydrocarbons in water of the Sinos River basin, Southern Brazil. Arch Environ Contam Toxicol 72(3):321–334CrossRefPubMedPubMedCentralGoogle Scholar
  14. Blume KK, Macedo JC, Meneguzzi A, Silva LB, Quevedo DM, Rodrigues MAR (2010) Water quality assessment of the Sinos River, Southern Brazil. Braz J Biol 70(4):1185–1193CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bolognesi C, Cirillo S (2014) Genotoxicity biomarkers in aquatic bioindicators. Curr Zool 60(2):273–284CrossRefGoogle Scholar
  16. Bolognesi C, Hayashi M (2011) Micronucleus assay in aquatic animals. Mutagenesis 26:205–2013CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bolognesi C, Perrone E, Roggieri P, Pampanin DM, Sciutto A (2006) Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquat Toxicol 78(Suppl 1):S93–S98CrossRefPubMedPubMedCentralGoogle Scholar
  18. Brasil (2005) National Environment Council—CONAMA Resolução CONAMA 357, de 2005. Available in: http://www.mma.gov.br/port/conama/res/res05/res35705.pdf. Accessed 21 Oct 2018
  19. Broeg K, Westernhagen HV, Zander S, Korting W, Koehler A (2005) The “bioeffect assessment index” (BAI): a concept for the quantification of effects of marine pollution by an integrated biomarker approach. Mar Pollut Bull 50:495–503CrossRefPubMedPubMedCentralGoogle Scholar
  20. Bueno-Krawczyk ACD, Guiloski IC, Piancini LDS, Azevedo JC, Ramsdorf WA, Ide AH, Guimarães ATB, Cestari MM, Silva AHC (2015) Multibiomarker in fish to evaluate a river used to water public supply. Chemosphere 135:257–264CrossRefPubMedPubMedCentralGoogle Scholar
  21. Bühler D, Marinowic R, Rodrigues MAS, Silva L (2012) Evaluation of genotoxicity and cytotoxicity of treated tannery wastewater in Southern Brazil. Int J Environ Technol Manag 15:114–123CrossRefGoogle Scholar
  22. Bühler D, Marinowic R, Barros MP, Silva L (2014) Genetic damage induced by water pollutants in the freshwater fish Hyphessobrycon luetkenii (Characidae) in a reservoir of the Canela National Forest, Brazil. J Freshw Ecol 29:295–299CrossRefGoogle Scholar
  23. Carrasco KR, Tilbury KL, Myers MS (1990) Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquatic Sci 47(11):2123–2136CrossRefGoogle Scholar
  24. Cassanegro MBB, Droste A (2017) Assessing the spatial pattern of a river water quality in southern Brazil by multivariate analysis of biological and chemical indicators. Braz J Biol 77(1):118–126CrossRefGoogle Scholar
  25. Çavas T, Ergene-Gozukara S (2003) Micronuclei, nuclear lesions and interphase silver-stained regions (AgNORs) as cytogenotoxic indicators in Oreochromis niloticus exposed to textile mill effluent. Mutat Res 538(1–2):81CrossRefPubMedPubMedCentralGoogle Scholar
  26. Chavan P, Kumar R, Joshi H, Kirubagaran R, Venugopalan VP (2017) Multimarker study of the effects of antifouling biocide on benthic organisms: results using Perna viridis as candidate species. Environ Sci Pollut Res 25(21):20407–20418CrossRefGoogle Scholar
  27. Comitesinos – Comitê de Gerenciamento da Bacia Hidrográfica do Rio dos Sinos (2009) Available in: http://www.comitesinos.com.br/planos-estudostecnicos-e-legislacao/1o-plano-de-bacia/. Accessed 29 June 2016
  28. Costa GM, Benvenuti T, Rubio MAK, Rodrigues MAS, Droste A (2014) Monitoramento químico e do potential genotóxico para o diagnóstico da qualidade de corpos hídricos. Rev Bras Ciências Ambient 32:65–74Google Scholar
  29. D’Costa A, Shyama SK, Kumar MKP (2017) Bioaccumulation of trace metals and total petroleum and genotoxicity responses in an edible fish population as indicators of marine pollution. Ecotoxicol Environ Safe 142:22–28CrossRefGoogle Scholar
  30. Dalzochio T, Rodrigues GZP, Simões LAR, Souza MS, Andriguetti NB, Silva GJH, Silva LB, Gehlen G (2018a) In situ monitoring of the Sinos River, southern Brazil: water quality parameters, biomarkers, and metal bioaccumulation in fish. Environ Sci Pollut Res Int 25(10):9485–9500CrossRefPubMedPubMedCentralGoogle Scholar
  31. Dalzochio T, Simões LAR, Souza MS, Rodrigues GZP, Schvambach LJ, Lehmann PCA, Gehlen G, Basso LB (2018b) Genotoxic effects on fish species and water quality parameters of two tributaries of the Sinos River, Southern Brazil. Int J Environ Technol Manage 21(3/4):161–173Google Scholar
  32. Erbe MCL, Ramsdorf WA, Vicari T, Cestari MM (2011) Toxicity evaluation of water samples collected near a hospital waste landfill through bioassays of genotoxicity piscine micronucleus test and comet assay in fish Astyanax and ecotoxicity Vibrio fischeri and Daphnia magna. Ecotoxicology 20:320–328CrossRefPubMedPubMedCentralGoogle Scholar
  33. Fasulo S, Mauceri A, Maisano M, Giannetto A, Parrino V, Gennuso F, D’Agata A (2013) Immunohistochemical and molecular biomarkers in Coris julis exposed to environmental pollutants. Ecotoxicol Environ Safe 73(5):873–882CrossRefGoogle Scholar
  34. Fenech M (2007) Cytokinesis-block micronucleus cytome assay. Nat Protoc 2(5):1084–1104CrossRefPubMedPubMedCentralGoogle Scholar
  35. Figueiredo JAS, Drumm E, Rodrigues MAS, Spilki FR (2010) The Rio dos Sinos watershed: an economic and social space and its interface with environmental status. Braz J Biol 70(S4):1131–1136CrossRefPubMedPubMedCentralGoogle Scholar
  36. Foy CD, Chancy RL, White MC (1978) The physiology of metal toxicity in plants. Ann Rev Plant Phys 29(1):511–566CrossRefGoogle Scholar
  37. Furnus GNA, Caffetti JD, García EM, Benítes MF, Pastori MC, Fenocchio AS (2014) Baseline micronuclei and nuclear abnormalities frequencies in native fishes from Paraná River (Argentina). Braz J Biol 74:217–221CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fuzinatto CF, Flohr L, Melegari SP, Matias WG (2013) Induction of micronucleus of Oreochromis niloticus exposed to waters from the Cubatão do Sul River, southern Brazil. Ecotoxicol Environ Safe 98:103–109CrossRefGoogle Scholar
  39. Gomes LC, Chippari-Gomes AR, Miranda TO, Pereira TM, Merçon J, Davel VC, Barbosa BV, Pereira ACH, Frossard A, Ramos JPL (2019) Genotoxicity effects on Geophagus brasiliensis fish exposed to Doce River water after the environmental disaster in the city of Mariana, MG, Brazil. Braz J Biol 79(4):659–664CrossRefPubMedPubMedCentralGoogle Scholar
  40. Gonzalez G, Crespo S, Brusle J (1993) Histo-cytological study of the liver of the cabrilla sea bass, Serranus cabrilla (Teleostei, Serranidae), an available model for marine fish experimental studies. J Fish Biol 43(3):363–373CrossRefGoogle Scholar
  41. Grisolia CK, Rivero CLG, Starling FLRM, Silva ICR, Barbosa AC, Dorea JG (2009) Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genet Mol Biol 32:138–143CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hatje V, Bidone ED, Maddock JL (1998) Estimation of the natural and anthropogenic components of heavy metal fluxes in fresh water Sinos River, Rio Grande do Sul State, South Brazil. Environ Technol 19(5):483–487CrossRefGoogle Scholar
  43. Hermes N, Schneider RCS, Molin DD, Riegel GZ, Costa AB, Corbellini VA, Torres JPM, Malm O (2013) Environmental pathways and human exposure to manganese in southern Brazil. An Acad Bras Ciênc 85(4):1275–1288CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hintzsche H, Hemmann U, Poth A, Utesch D, Lott J, Stopper H (2017) Fate of micronuclei and micronucleated cells. Mutat Res 771:85–98CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hook SE (2010) Promise and progress in environmental genomics: a status report on the applications of microarray studies in ecologically relevant fish species. J Fish Biol 77:1999–2022CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hook SE, Gallagher EP, Batley GE (2014) The role of biomarkers in the assessment of aquatic ecosystem health. Integr Environ Assess Manag 10(3):327–341CrossRefPubMedPubMedCentralGoogle Scholar
  47. Instituto Brasileiro de Geografia e Estatística e IBGE (2010) Indicadores de Desenvolvimento Sustentável e Brasil. Available in: http://www.ibge.gov.br/home/geociencias/recursosnaturais/ids/default_2010.shtm. Accessed 20 Dec 2016
  48. Jesus IS, Cestari MM, Bezerra MA, Affonso PRAM (2016) Genotoxicity effects in freshwater fish from a Brazilian impacted river. Bull Environ Contam Toxicol 96:490–495CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kieling-Rubio MA, Benvenuti T, Costa GM, Petry CT, Rodrigues MA, Schmitt JL, Droste A (2015) Integrated environmental assessment of streams in the Sinos River basin in the state of Rio Grande do Sul, Brazil. Braz J Biol 75(2):S105–S113CrossRefGoogle Scholar
  50. Kirsch-Volders M, Plas G, Elhajouji A, Lukamowicz M, Gonzalez L, Vande Loock K, Decordier I (2011) The in vitro MN assay in 2011: origin and fate, biological significance, protocols, high throughput methodologies and toxicological relevance. Arch Toxicol 85(8):873–899CrossRefPubMedPubMedCentralGoogle Scholar
  51. Konzen GB, Figueiredo JAS, Quevedo DM (2015) History of water quality parameters - a study on the Sinos River/Brazil. Braz J Biol 75(S2):S1–S10CrossRefGoogle Scholar
  52. Kosanovic M, Hasan MY, Subramanian D, Al Ahbabi AAF, Al Kathiri OAA, Aleassa EMAA, Adem A (2007) Influence of urbanization of the western coast of the United Arab Emirates on trace metal content in muscle and liver of wild Red-spot emperor (Lethrinus lentjan). Food Chem Toxicol 45(11):2261–2266CrossRefPubMedPubMedCentralGoogle Scholar
  53. Leme DM, Marin-Morales MA (2009) Allium cepa test in environmental monitoring: a review on its application. Mutat Res 682:71–81CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lemos CT, Rodel PM, Terra NR, Oliveira CD, Erdtmann B (2007) River water genotoxicity evaluation using micronucleus assay in fish erythrocytes. Ecotoxicol Environ Safe 66:391–401CrossRefGoogle Scholar
  55. Lemos CT, Iranço FA, Oliveira NCD, Souza GD, Fachel JMG (2008) Biomonitoring of genotoxicity using micronuclei assay in native population of Astyanax jacuhiensis (Characiformes: Characidae) at sites under petrochemical influence. Sci Total Environ 406:337–343CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lima LBD, Morais PB, Andrade RLT, Mattos LV, Moron SE (2018) Use of biomarkers to evaluate the ecological risk of xenobiotics associated with agriculture. Environ Pollut 237:611–624CrossRefPubMedPubMedCentralGoogle Scholar
  57. Linde-Arias AR, Inácio AF, Albuquerque C, Freire MM, Moreira JC (2008) Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian river. Sci Total Environ 399(1–3):186–192CrossRefPubMedPubMedCentralGoogle Scholar
  58. Loro VL, Murussi C, Menezes C, Leitemperger J, Severo E, Guerra L, Costa M, Perazzo GX, Zanella R (2015) Spatial and temporal biomarkers responses of Astyanax jacuhiensis (Cope, 1894) (Characiformes: Characidae) from the middle Rio Uruguai, Brazil. Neotrop Ichthyol 13:569–578CrossRefGoogle Scholar
  59. Lucena CA, Soares HG (2016) Review of species of the Astyanax bimaculatus “caudal peduncle spot” subgroup sensu Garutti & Langeani (Characiformes, Characidae) from the rio La Plata and rio São Francisco drainages and coastal systems of southern Brazil and Uruguay. Zootaxa 4072:101–125CrossRefPubMedPubMedCentralGoogle Scholar
  60. Marcato ACC, Yabuki AT, Fontanetti CS (2014) Nickel exposure promotes osmoregulatory disturbances in Oreochromis niloticus gills: histopathological and energy dispersive spectrometry analysis. Environ Sci Poll Res Int 21(22):13095–13102CrossRefGoogle Scholar
  61. Marcon AE, Ferreira DM, Moura MFV, Campos TFC, Amaral VS, Agnez-Lima LF, Medeiros SBR (2010) Genotoxic analysis in aquatic environment under influence of cyanobacteria, metal and radioactivity. Chemosphere 81:773–780CrossRefPubMedPubMedCentralGoogle Scholar
  62. Matos LA, Cunha ACS, Sousa AA, Maranhão JPR, Santos NRS, Gonçalves MMC, Dantas SMMM, Sousa JMC, Peron AP, Silva FCC, Alencar MVOB, Islam T, Aguiar RPS, Melo-Cavalcante BCC, Junior HFJ (2017) The influence of heavy metals on toxicogenic damage in a Brazilian tropical river. Chemosphere 185:852–859CrossRefPubMedPubMedCentralGoogle Scholar
  63. Mazzeo DEC, Matsumoto ST, Levy CE, Angelis DF, Marin-Morales MA (2013) Application of micronucleus test and comet assay to evaluate BTEX biodegradation. Chemosphere 90:1030–1036CrossRefPubMedPubMedCentralGoogle Scholar
  64. Nunes EA, Lemos CL, Gavronski L, Moreira TN, Oliveira NCD, Silva J (2011) Genotoxic assessment on river water using different biological systems. Chemosphere 84:47–53CrossRefPubMedPubMedCentralGoogle Scholar
  65. Oliveira MTG, Rolim SBA, Mello-Farias PC, Meneguzzi A, Lutckmeier C (2008) Industrial pollution of environmental compartments in the Sinos River Valley, RS, Brazil: geochemical-biogeochemical characterization and remote sensing. Water Air Soil Pollut 192:183–198CrossRefGoogle Scholar
  66. Ossana NA, Castane PM, Salibian A (2013) Use of lithobates catesbeianus tadpoles in a multiple biomarker approach for the assessment of water quality of the Reconquista river (Argentina). Arch Environ Contam Toxicol 65:486–497CrossRefPubMedPubMedCentralGoogle Scholar
  67. Ossana NA, Eissa BL, Baudou FG, Castañé PM, Soloneski S, Ferrari L (2016) Multibiomarker response in ten spotted live-bearer fish Cnesterodon decemmaculatus (Jenyns, 1842) exposed to Reconquista river water. Ecotoxicol Environ Safe 133:73–81CrossRefGoogle Scholar
  68. Palhares D, Grisolia CK (2002) Comparison between the micronucleus frequencies of kidney and gill erythrocytes in tilapia fish, following mitomycin C treatment. Gen Mol Biol 25(3):281–284CrossRefGoogle Scholar
  69. Rodrigues APC, Maciel PO, Silva LLCP, Albuquerque C, Inácio AF, Freire M, Linde AR, Almosny NRP, Andreata JV, Bidone ED, Castilhos ZC (2010) Biomarkers for mercury exposure in tropical estuarine fish. J Braz Society Ecotoxicol 5(1):9–18CrossRefGoogle Scholar
  70. Scalon MCS, Rechenmacher C, Siebel AM, Kayser ML, Rodrigues MT, Maluf SW, Rodrigues MAS, Silva LB (2010) Evaluation of Sinos River water genotoxicity using the comet assay in fish. Braz J Biol 70(4):1217–1222CrossRefPubMedPubMedCentralGoogle Scholar
  71. Sena AR, Machado A, Barbosa SA, Santos LO, Santos MN (2018) Avaliação da qualidade da água do Rio Pitanga, São Cristóvão/SE. Interfaces Científicas-Saúde e Ambiente 6(3):63–74Google Scholar
  72. Seriani R, Abessa DMS, Kirschbaum AA, Pereira CDS, Ranzani-Paiva MJT, Assunção A, Silveira FL, Romano P, Mucci JLN (2012) Water toxicity and cyto-genotoxcity biomarkers in the fish Oreochromis niloticus (Cichlidae). J Braz Soc Ecotoxicol 7(2):67–72CrossRefGoogle Scholar
  73. Seriani R, Abessa DMS, Moreira LB, Cabrera JPG, Sanches JQ, Silva CLS, Amorim FA, Rivero DHRF, Silva FL, Fitorra LS, Carvalho-Oliveira R, Macchione M, Ranzani-Paiva MJT (2015) In vitro mucus transportability, cytogenotoxicity, and hematological changes as non-destructive physiological biomarkers in fish chronically exposed to metals. Ecotoxicol Environ Safe 112:162–168CrossRefGoogle Scholar
  74. Souza TS, Fontanetti CS (2006) Micronucleus test and observations of nuclear alterations in erythrocytes of Nile tilapia to waters affected by refinery effluent. Mutat Res 605:87–93CrossRefGoogle Scholar
  75. Souza MS, Rodrigues GZP, Dalzochio T, Goldoni A, Simões LAR, Gehlen G, Silva LB (2016) Avaliação da qualidade da água do Rio dos Sinos (Brasil) por meio do teste de micronúcleos em Cyprinus carpio e de análises físico-químicas e microbiológicas. Acta Toxicol Argent 24(3):193–199Google Scholar
  76. Steffens C, Klauck CR, Benvenuti T, Silva LB, Rodrigues MAS (2015) Water quality assessment of the Sinos River, RS, Brazil. Braz J Biol 75(4):62–67CrossRefGoogle Scholar
  77. Streck EV, Kämpf N, Dalmolin RSD, Klamt E, Nascimento PC, Schneider P, Giasson E, Pinto LFS (2008) Solos do Rio Grande do Sul, 2nd edn. EMATER/RS, Porto Alegre, 222 pGoogle Scholar
  78. Tabrez S, Shakil S, Urooj M, Damanhouri GA, Abuzenadah AM, Ahmad M (2011) Genotoxicity testing and biomarker studies on surface waters: an overview of the techniques and their efficacies. J Environ Sci Health C 29:250–275CrossRefGoogle Scholar
  79. Terra NR, Feiden IR, Fachel JMG, Lemos CT, Nunes EA (2008) Ecotoxicological evaluation of sediment and water samples from Sinos River, Rio Grande do Sul, Brazil, using Daphnia magna and V79 cells. Acta Limnol Bras 20(1):63–72Google Scholar
  80. Trapp J, Armengaud J, Salvador A, Chaumot A, Geffard O (2014) Next-generation proteomics: toward customized biomarkers for environmental biomonitoring. Environ Sci Technol 48:13560–13572CrossRefPubMedPubMedCentralGoogle Scholar
  81. Udroiu I (2006) The micronucleus test in piscine erythrocytes. Aquat Toxicol 79(2):201–204CrossRefPubMedPubMedCentralGoogle Scholar
  82. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:149–157Google Scholar
  83. Velusamy A, Kumar PS, Ram A, Chinnadurai S (2014) Bioaccumulation of heavy metals in commercially important marine fishes from Mumbai Harbor, India. Mar Pollut Bull 81(1):218–224CrossRefPubMedPubMedCentralGoogle Scholar
  84. Vieira CED, Almeida MS, Galindo BA, Pereira L, Martinez CBR (2014) Integrated biomarker response index using a Neotropical fish to assess the water quality in agricultural areas. Neotrop Ichthyol 12:153–164CrossRefGoogle Scholar
  85. Vieira CED, Costa PG, Lunardelli B, Oliveira LF, Cabrera LC, Risso WE, Primel EG, Meletti PC, Fillmann G, Martinez CBR (2016) Multiple biomarker responses in Prochilodus lineatus subjected to short-term in situ exposure to streams from agricultural areas in Southern Brazil. Sci Total Environ 542:44–56CrossRefPubMedPubMedCentralGoogle Scholar
  86. WHO International Programme on Chemical Safety (IPCS) (1993) Biomarkers and risk assessment: concepts and principles, Environmental Health Criteria 155. World Health Organization, GenevaGoogle Scholar
  87. Zapata LM, Bock BC, Orozco LY, Palacio JA (2016) Application of the micronucleus test and comet assay in Trachemys callirostris erythrocytes as a model for in situ genotoxic monitoring. Ecotoxicol Environ Safe 127:108–116CrossRefGoogle Scholar
  88. Zegura B, Heath E, Cernosa A, Filipic M (2009) Combination of in vitro bioassays for the determination of cytotoxic and genotoxic potential of wastewater, surface water and drinking water samples. Chemosphere 75:1453–1460CrossRefPubMedPubMedCentralGoogle Scholar
  89. Zoppas FM, Bernardes AM, Meneguzzi Á (2016) Parâmetros operacionais na remoção biológica de nitrogênio de águas por nitrificação e desnitrificação simultânea. Bio Rev Engenharia Sanitária 21(1):29–42Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Thaís Dalzochio
    • 1
  • Natália Bordin Andriguetti
    • 1
  • Leonardo Airton Ressel Simões
    • 1
  • Günther Gehlen
    • 1
  • Luciano Basso da Silva
    • 1
  1. 1.Programa de Pós-graduação em Qualidade Ambiental, Universidade FeevaleNovo HamburgoBrazil

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