Abstract
Freshwater and marine water bodies receive chemical contaminants from industrial, agricultural, urban, and domestic wastes. Eco-genotoxicity assays are useful tools to assess the cumulative genotoxicity of these pollutants. Fish are suitable indicators for biomonitoring of mutagenic and carcinogenic pollution.
In this review, we present a complete overview of the studies performed so far using the micronucleus test in peripheral erythrocytes of fish exposed to polluted water. We have listed all the species of fish used and the geographical distribution of the investigations. We have analyzed and discussed all technical aspects of using this test in fish, as well as the advantages and disadvantages of the different experimental protocols. We have reported the results of all studies. This assay has become, for years, one of the simplest, fastest, and most cost-effective for assessing genotoxic risk in aquatic environments. However, there are still several factors influencing the variability of the results. Therefore, we have given indications and suggestions to achieve a standardization of experimental procedures and ensure uniformity of future investigations.
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References
Abdel-Khalek AA (2015) Antioxidant responses and nuclear deformations in freshwater fish, Oreochromis niloticus, facing degraded environmental conditions. Bull Environ Contam Toxicol 94:701–708
Abdel-Khalek AA, Dajem SB, Morsy K (2020) The long-term exposure to discharges of Sabal drain induces genotoxic effects on Oreochromis niloticus. Bull Environ Contam Toxicol 104:858–863
Abujamara LD, Seriani R, Ranzani-Paiva MJ, Moreira LB, Abessa DMS, Pereira CDS (2011) Análise de parâmetros citogenotóxicos da corvina, Micropogonias furnieri, provenientes de dois estuários da Baixada Santista, SP. Rev Ceciliana Dez 3:17–20 (in Portuguese)
Acolas M-L, Davail B, Gonzalez P, Jean S, Clérandeau C, Morin B, Gourves P-Y, Daffe G, Labadie P, Perrault A, Lauzent M, Pierre M, Le Barh R, Baudrimont M, Peluhet L, Le Menach K, Budzinski H, Rochard E, Cachot J (2020) Health indicators and contaminant levels of a critically endangered species in the Gironde estuary, the European sturgeon. Environ Sci Pollut Res 27:3726–3745
Adam ML, Torres RA, Sponchiado G, Motta TS, Oliveira CMR, Carvalho-Filho MA, Correia MTS (2010) Environmental degradation at a public park in Southern Brazil as revealed through a genotoxicity test (MN) on peripheral blood cells from Poecilia vivipara (Teleostei). Water Air Soil Pollut 211:61–68
Aguiar LL, Tonon CB, Nunes ET, Braga ACA, Neves MA, David JAO (2016) Mutagenic potential of fine wastes from dimension stone industry. Ecotoxicol Environ Saf 125:116–120
Ahmad W, Ali NM, Farah AM, Ateeq B (2002) Computerized automated morphometric assay including frequency estimation of pentachlorophenol induced nuclear anomalies (micronucleus) in catfish Heteropneustes fossilis. Chromosoma 110:570–574
Ali FK, El-Shehawi AM, Seehy MA (2008) Micronucleus test in fish genome: a sensitive monitor for aquatic pollution. Afr J Biotechnol 7:606–612
Aliko V, Morina V, Sula E (2015) Cellular and nuclear alterations of carp fish (Cyprinus carpio) erythrocytes as sensitive biomarkers of citotoxicity and genotoxicity of Sitnica River waters (Kosovo). Aktet 8:163–168
Alimba CG, Bakare AA (2016) In vivo micronucleus test in the assessment of cytogenotoxicity of landfill leachates in three animal models from various ecological habitats. Ecotoxicology 25:310–319
Alimba CG, Ajiboye RD, Fagbenro OS (2017) Dietary ascorbic acid reduced micronucleus and nuclear abnormalities in Clarias gariepinus (Burchell 1822) exposed to hospital effluent. Fish Physiol Biochem 43:1325–1335
Alimba CG, Adekoya KO, Soyinka OO (2019) Exposure to effluent from pharmaceutical industry induced cytogenotoxicity, hematological and histopathological alterations in Clarias gariepinus. Excli J 18:63–78
Al-Sabti K (1986a) Clastogenic effects of five carcinogenic mutagenic chemicals on the cells of the common carp, Cyprinus carpio L. Comp Biochem Physiol C 85:5–9
Al-Sabti K (1986b) Comparative micronucleated erythrocyte cell induction in three cyprinids by five carcinogenic-mutagenic chemicals. Cytobios 47:147–154
Al-Sabti K (1991) Handbook of genotoxic effects and fish chromosomes. J Stefan Institute Press, Yugoslavia
Al-Sabti K (1992a) Micronuclei induction in pike (Esox lucius) in Swedish lakes contaminated with radiocesium. Cytobios 70:27–32
Al-Sabti K (1992b) Monitoring the genotoxicity of radiocontaminants in Swedish lakes by fish micronuclei. Cytobios 70:101–106
Al-Sabti K, Hardig J (1990) Micronucleus test in fish for monitoring the genotoxic effects of industrial waste products in the Baltic Sea, Sweden. Comp Biochem Physiol C 97:179–182
Al-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343:121–135
Al-Sabti K, Franko M, Andrijanic B, Knez S, Stegnar P (1994) Chromium-induced micronuclei in fish. J Appl Toxicol 14:333–336
Amado LL, Robaldo RB, Geracitano LA, Monserrat JM, Bianchini A (2006a) Biomarkers of exposure and effect in the Brazilian flounder Paralichthys orbignyanus (Teleostei: Paralichthyidae) from the Patos Lagoon estuary (Southern Brazil). Mar Pollut Bull 52:207–213
Amado LL, Rosa CE, Leite AM, Moraes L, Pires WV, Pinho GLL, Martins CMG, Robaldo RB, Nery LEM, Monserrat JM, Bianchini A, Martinez PE, Geracitano LA (2006b) Biomarkers in croakers Micropogonias furnieri (Teleostei: Sciaenidae) from polluted and non-polluted areas from the Patos Lagoon estuary (Southern Brazil): evidences of genotoxic and immunological effects. Mar Pollut Bull 52:199–206
Andrade VM, Silva J, Silva FR, Heuser VD, Dias JF, Yoneama ML, Freitas TRO (2004) Fish as bioindicators to assess the effects of pollution in two southern brazilian rivers using the comet assay and micronucleus test. Environ Mol Mutagen 44:459–468
Anifowoshe AT, Oladipo SO, Owolodun OA, Akinseye MK, Olafimihan TF, Sidiq AG, Muhammed AA, Asa TA, Mustapha MK (2018) Ecogenotoxicogical assessments of some selected fish species from Apodu Reservoir, Malete, North Central, Nigeria. Manila J Sci 11:1–14
Araldi RP, Melo TC, Mendes TB, Sà Jùnior PL, Nozima BHN, Ito ET, Carvalho RF, Souza EB, Stocco RC (2015) Using the comet and micronucleus assay for genotoxicity studies: a review. Biomed Pharmacother 72:74–82
Arantes ACR, Adam ML, Souza JRB, Bastos LP, Jacobina UP, Torres RA (2016) Frequency of fish micronuclei to diagnose aquatic environmental conditions from Brazilian megacities: a case study of Iguaçu river, Southern Brazil. R Bras Bioci 14:111–116
Arslan Ă–C, Parlak H (2017) Micronucleus test good biomarker for determination of genetic changes in aquatic organisms. J Aquat Pollut Toxicol 1:18
Arslan ÖC, Parlak H, Katalay S, Boyacioglu M, Karaaslan MA, Guner H (2010) Detecting micronuclei frequency in some aquatic organisms for monitoring pollution of Izmir Bay (Western Turkey). Environ Monit Assess 165:55–56
Arslan ÖC, Boyacioglu M, Parlak H, Katalay S, Karaaslan MA (2015) Assessment of micronuclei induction in peripheral blood and gill cells of some fish species from Aliaga Bay Turkey. Mar Pollut Bull 94:48–54
Asllani FH, Schürz M, Bresgen N, Eckl PM, Alija AJ (2019) Genotoxicity risk assessment in fish (Rutilus rutilus) from two contaminated rivers in the Kosovo. Sci Total Environ 676:429–435
Ayllón F, Suciu R, Gephard S, Juanes F, Garcia-Vazquez E (2000) Conventional armament wastes induce micronuclei in wild brown trout Salmo trutta. Mutat Res 470:169–176
Ayoola SO, Bassey BO, Alimba CG, Ajani EK (2012) Textile effluent induced genotoxic effect and oxidative stress in Clarias gariepinus. Pak J Biol Sci 15:804–812
Azevedo JS, Braga ES, Ribeiro CAO (2012) Nuclear abnormalities in erythrocytes and morphometric indexes in the catfish Cathorops spixii from different sites on the Southeastern Brazilian coast. Braz J Oceanogr 60:323–330
Bagdonas E, Bukelskis E, Lazutka JR (2003) Frequency of micronucleated erythrocytes in wild fish from natural freshwater body. Ekologija 1:67–71
Barbee GC, Barich J, Duncan B, Bickham JW, Matson CW, Hintze CJ, Autenrieth RL, Zhou G-D, McDonald TJ, Cizmas L, Norton D, Donnelly KC (2008) In situ biomonitoring of PAH-contaminated sediments using juvenile coho salmon (Oncorhynchus kisutch). Ecotoxicol Environ Saf 71:454–464
Barbosa JS, Cabral TM, Ferreira DN, Agnez-Lima LF, Medeiros SRB (2010) Genotoxicity assessment in aquatic environment impacted by the presence of heavy metals. Ecotoxicol Environ Saf 73:320–325
Baršienė J, Lazutka J, Syvokiene J, Dedonyte V, Rybakovas A, Bagdonas E, Bjornstad A, Andersen OK (2004) Analysis of micronuclei in blue mussels and fish from the Baltic and North Seas. Environ Toxicol 19:365–371
Baršienė J, Lehtonen KK, Koehler A, Broeg K, VuorinenPJ LT, Pempkowiak J, Syvokiene J, Dedonyte V, Rybakovas A, Repecka R, Vuontisjärvi H, Kopecka J (2006) Biomarker responses in flounder (Platichthys flesus) and mussel (Mytilus edulis) in the Klaipeda-Butinge area (Baltic Sea). Mar Pollut Bull 53:422–436
Baršienė J, Rybakovas A, Lang T, Grygiel W, Andreikenaite L, Michailovas A (2012) Risk of environmental genotoxicity in the Baltic Sea over the period of 2009-2011 assessed by micronuclei frequencies in blood erythrocytes of flounder (Platichthys flesus), herring (Clupea harengus) and eelpout (Zoarces viviparus). Mar Environ Res 77:35–42
Baršienė J, Rybakovas A, Lang T, Andreikenaite L, Michailovas A (2013) Environmental genotoxicity and cytotoxicity levels in fish from the North Sea offshore region and Atlantic coastal waters. Mar Pollut Bull 68:106–116
Baršienė J, Butrimavičienė L, Rybakovas A, Grygiel W, Lang T, Michailovas A, Jackunas T (2014) Environmental genotoxicity and cytotoxicity in flounder (Platichthys flesus), herring (Clupea harengus) and Atlantic cod (Gadus morhua) from chemical munitions dumping zones in the southern Baltic Sea. Mar Environ Res 96:56–67
Baršienė J, Butrimavičienė L, Michailovas A, Grygiel W (2015) Assessing the environmental genotoxicity risk in the Baltic Sea: frequencies of nuclear buds in blood erythrocytes of three native fish species. Environ Monit Assess 187:4078–4089
Baršienė J, Butrimavičienė L, Grygiel W, Stunžėnas V, Valskienė R, Greiciūnaitė J, Stankevičiūtė M (2016) Environmental genotoxicity assessment along the transport routes of chemical munitions leading to the dumping areas in the Baltic Sea. Mar Pollut Bull 103:45–53
Başımoğlu Koca Y, Koca S, Yıldız S, Gürcü B, Osanç E, Tunçbaş O, Aksoy G (2005) Investigation of histopathological and cytogenetic effects on Lepomis gibbosus (Pisces: Perciformes) in the Çine stream (Aydın/Turkey) with determination of water pollution. Environ Toxicol 20:560–571
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 different anthropogenic activities. Chemosphere 164:134–141
Baudou FG, Ossana NA, Castañé PM, Mastrángelo MM, González Núñez AA, Palacio MJ, Ferrari L (2019) Use of integrated biomarker indexes for assessing the impact of receiving waters on a native neotropical teleost fish. Sci Total Environ 650:1779–1786
Beaton ED, Gosselin I, Festarini A, Gagnaire B, Farrow F, Cavalié I, Shultz C, Kim SB, Walsh S, Chen HQ, Adam-Guillermin C, Stuart M (2019) Correlated responses for DNA damage, phagocytosis activity and lysosomal function revealed in a comparison between field and laboratory studies: fathead minnow exposed to tritium. Sci Total Environ 662:990–1002
Belfiore NM, Anderson SL (2001) Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat Res 489:97–122
Benincá C, Ramsdorf W, Vicari T, Ribeiro CAO, Almeida MI, Assis HCS, Cestari MM (2012) Chronic genetic damages in Geophagus brasiliensis exposed to anthropic impact in Estuarine Lakes at Santa Catarina Coast – Southern of Brazil. Environ Monit Assess 184:2045–2056
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(Suppl. 2):S63–S67
Bessa ML, Antunes SC, Pereira R, Gonçalves FJM, Nunes B (2016) Multibiomarker toxicity characterization of uranium mine drainages to the fish Carassius auratus. Environ. Sci Pollut Res 23:13355–13367
Beyer J, Petersen K, Song Y, Ruus A, Grung M, Bakke T, Tollefsen KE (2014) Environmental risk assessment of combined effects in aquatic ecotoxicology: a discussion paper. Mar Environ Res 96:81–91
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(Suppl. 2):S68–S74
Bickham JW, Sandhu S, Hebert PDN, Chikhi L, Athwal R (2000) Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat Res 463:33–51
Boettcher M, Grund S, Keiter S, Kosmehl T, Reifferscheid G, Seitz N, Rocha PS, Hollert H, Braunbeck T (2010) Comparison of in vitro and in situ genotoxicity in the Danube River by means of the comet assay and the micronucleus test. Mutat Res 700:11–17
Bogoni JA, Armiliato N, Araldi-Favassa CT, Techio VH (2014) Genotoxicity in Astyanax bimaculatus (Twospot Astyanax) exposed to the waters of Engano River (Brazil) as determined by micronucleus tests in erythrocytes. Arch Environ Contam Toxicol 66:441–449
Bolognesi C, Hayashi M (2011) Micronucleus assay in aquatic animals. Mutagenesis 26:205–213
Bolognesi C, Perrone E, Roggieri P, Pampanin DM, Sciutto A (2006a) Assessment of micronuclei induction in perypheral blood erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquat Toxicol 78S:S93–S98
Bolognesi C, Perrone E, Roggieri P, Sciutto A (2006b) Bioindicators in monitoring long term genotoxic impact of oil spill: haven case study. Mar Environ Res 62:S287–S291
Bombail V, Dennis A, Gordon E, Batty J (2001) Application of the comet and micronucleus assay to butterfish (Pholis gunnellus) erythrocytes from the Firth of Forth, Scotland. Chemosphere 44:383–392
Bonnineau C, Moeller A, Barata C, Proia L, Sans-Piché F, Schmitt-Jansen M, Guasch H, Segner H (2012) Advances in the multibiomarker approach for risk assessment in aquatic ecosystems. In: Guasch H, Ginebreda A, Geiszinger A (eds) The handbook of environmental chemistry v.19 — emergency and priority pollutants in rivers. Springer, Berlin, pp 147–179
Brack W, Ait-Aissa S, Backhaus T, Dulio V, Escher BI, Faust M, Hilscherova K, Hollender J, Hollert H, MĂĽller C, Munthe J, Posthuma L, Seiler T-B, Slobodnik J, Teodorovic I, Tindall AJ, de AragĂŁo UG, Zhang X, Altenburger R (2019) Effect-based methods are key. The European Collaborative Project SOLUTIONS recommends integrating effect-based methods for diagnosis and monitoring of water quality. Environ Sci Eur 31:10
Braham RP, Blazer VS, Shaw CH, Mazik PM (2017) Micronuclei and other erythrocyte nuclear abnormalities in fishes from the Great Lakes Basin, USA. Environ Mol Mutagen 58:570–581
Bresler V, Bissinger V, Dizer AAH, Sturm A, Kratke R, Fishelson L, Hansen P-D (1999) Marine molluscs and fish as biomarkers of pollution stress in littoral regions of the Red Sea, Mediterranean Sea and North Sea. Helgol Mar Res 53:219–243
BĂĽcker A, Conceição MB (2012) Genotoxicity evaluation of tilapia (Oreochromis niloticus) exposed to waters from two sites of ItajaĂ-Açu River (SC, Brazil). J Braz Soc Ecotoxicol 7:51–56
Bühler D, Marinowic DR, Barros MP, Silva LB (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 29:295–299
Buschini A, Martino A, Gustavino B, Monfrinotti M, Poli P, Rossi C, Santoro M, Dörr AJM, Rizzoni M (2004) Comet assay and micronucleus test in circulating erythrocytes of Cyprinus carpio specimens exposed in situ to lake waters treated with disinfectants for potabilization. Mutat Res 557:119–129
Butrimavičienė L, Baršienė J, Greiciūnaitė J, Stankevičiūtė M, Valskienė R (2018) Environmental genotoxicity and risk assessment in the Gulf of Riga (Baltic Sea) using fish, bivalves, and crustaceans. Environ Sci Pollut Res 25:24818–24828
Cajaraville MP, Hauser L, Carvalho G, Hylland K, Olabarrieta I, Lawrence AJ, Lowe D, Goksøyr A (2003) Genetic damage and the molecular/cellular response to pollution. In: Lawrence AJ, Hemingway KL (eds) Effects of pollution on fish: molecular effects and population responses. Blackwell Science, Oxford, pp 14–82
Campana MA, Panzeri AM, Escalante AH, Moreno VJ, Dulout FN (2001) Micronucleus test in fish from a pampasic pond (Argentina): an estimation of the presence of genotoxic compounds. J Environ Pathol Toxicol Oncol 20:325–331
Campos Júnior EO, Pereira BB, Morelli S, Pavanin EV, Pavanin LA (2014) Biological monitoring and B chromosome frequency in Bagre (Rhamdia quelen) in Southeast Brazil. Environ Toxicol Pharmacol 38:510–517
Campos Júnior EO, Pereira BB, Morelli S (2015) Monitoring genotoxicity potential in the Mumbuca. J Toxicol Environ Health A 78:1277–1287
Campos JĂşnior EO, Silva Oliveira RG, Pereira BB, Souto HN, Campos CF, Nepomuceno JC, Morelli S (2016) Assessment of genotoxic, mutagenic, and recombinogenic potential of water resources in the ParanaĂba River Basin of Brazil: a case study. J Toxicol Environ Health A 79:1190–1200
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 Aquat Sci 47:2123–2136
Carrola J, Santos N, Rocha MJ, Fontainhas-Fernandes A, Pardal MA, Monteiro RA, Rocha E (2014) Frequency of micronuclei and of other nuclear abnormalities in erythrocytes of the grey mullet from the Mondego, Douro and Ave estuaries – Portugal. Environ Sci Pollut Res 21:6057–6068
Carvalho-Neta RNF, Sousa DBP, Sobrinho ICM, Horton EY, Almeida ZS, Tchaicka L, Sousa AL (2015) Genotoxic and hematological parameters in Colossoma macropomum (Pisces, Serrasalmidae) as biomarkers for environmental impact assessment in a protected area in northeastern Brazil. Environ Sci Pollut Res 22:15994–16003
Castaño A, Bols N, Braunbeck T, Dierickx P, Halder M, Halder M, Kawahara K, Lee LE, Mothersill C, Pärt P, Repetto G, Sintes JR, Rufli H, Smith R, Wood C, Segner H (2003) The use of fish cells in ecotoxicology. The report and recommendations of ECVAM Workshop 47. Altern Lab Anim 31:317–351
Castilhos ZC, Almonsy N, Souto PS, Pereira da Silva LCC, Linde AR, Bidone ED (2004) Bioassessment of ecological risk of amazonian ichthyofauna to mercury. Bull Environ Contam Toxicol 72:671–679
Castro D, Mieiro CL, Coelho JP, Guilherme S, Marques A, Santos MA, Duarte AC, Pereira E, Pacheco M (2018) Addressing the impact of mercury estuarine contamination in the European eel (Anguilla anguilla L., 1758) – an early diagnosis in glass eel stage based on erythrocytic nuclear morphology. Mar Pollut Bull 127:733–742
Çavas T, Ergene-Gözükara S (2003) Micronuclei, nuclear lesions and interphase silver-stained nucleolar organizer regions (AgNORs) as cyto-genotoxicity indicators in Oreochromis niloticus exposed to textile mill effluent. Mutat Res 538:81–91
Çavas T, Ergene-Gözükara S (2005a) Micronucleus test in fish cells: a bioassay for in situ monitoring of genotoxic pollution in the marine environment. Environ Mol Mutagen 46:64–70
Çavas T, Ergene-Gözükara S (2005b) Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat Toxicol 74:264–271
Chamberland K, Lindroth BA, Whitaker B (2002) Genotoxicity in Androscoggin river smallmouth bass. Northeast Nat 9:203–212
Cheng C-H, Yang F-F, Liao S-A, Miao Y-T, Ye C-X, Wang A-L, Tan J-W, Chen X-Y (2015) High temperature induces apoptosis and oxidative stress in pufferfish (Takifugu obscurus) blood cells. J Therm Biol 53:172–179
Cheong HSJ, Seth I, Joiner MC, Tucker JD (2013) Relationships among micronuclei, nucleoplasmic bridges and nuclear buds within individual cells in the cytokinesis-block micronucleus assay. Mutagenesis 28:433–440
Claxton LD, Houk VS, Hughes TJ (1998) Genotoxicity of industrial wastes and effluents. Mutat Res 410:237–243
Coimbra RSC, Mascarenhas MS, Saraiva VB, Santos CR, Lopes RM, Hauser-Davis RA, Oliveira VPS, Molisani MM, Almeida MG, Rezende CE, Carvalho CEV, Oliveira MM (2018) Metal loads and biomarker suite responses in a tropical carnivorous fish indicative of anthropogenic impacts in a Southeastern Brazilian lagoon. Environ Monit Assess 190:564
Colin N, Porte C, Fernandes D, Barata C, Padròs F, Carrassòn M, Monroy M, Cano-Rocabayera O, Sostoa A, Piña B, Maceda-Veiga A (2016) Ecological relevance of biomarkers in monitoring studies of macro-invertebrates and fish in Mediterranean rivers. Sci Total Environ 540:307–323
Corredor-Santamaria W, GĂłmez MS, Velasco-Santamaria YM (2016) Using genotoxic and haematological biomarkers as an evidence of environmental contamination in the Ocoa River native fish, Villavicencio-Meta, Colombia. Springerplus 5:351
Costa PM, Costa MH (2007) Genotoxicity assessment in fish peripheral blood: a method for a more efficient analysis of micronuclei. J Fish Biol 71(Suppl A):148–151
Costa PM, Lobo J, Caeiro S, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, Costa MH (2008) Genotoxic damage in Solea senegalensis exposed to sediments from the Sado Estuary (Portugal): effects of metallic and organic contaminants. Mutat Res 654:29–37
Costa PM, Neuparth TS, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, Costa MH (2011) Assessment of the genotoxic potential of contaminated estuarine sediments in fish peripheral blood: laboratory versus in situ studies. Environ Res 111:25–36
Costa PM, Caeiro S, Vale C, DelValls TA, Costa MH (2012) Can the integration of multiple biomarkers and sediment geochemistry aid solving the complexity of sediment risk assessment? A case study with a benthic fish. Environ Pollut 161:107–120
Cotelle S, Ferard JF (1999) Comet assay in genetic ecotoxicology: a review. Environ Mol Mutagen 34:246–255
Cuevas N, Zorita I (2018) Baseline levels of environmental genotoxicity and potential confounding factors using common sole (Solea solea) as sentinel organism. Mar Environ Res 138:1–8
D’Costa A, Shyama SK, Praveen Kumar MK (2017) Bioaccumulation of trace metals and total petroleum and genotoxicity responses in an edible fish population as indicators of marine pollution. Ecotoxicol Environ Saf 142:22–28
Dalzochio T, Ressel Simões LA, de Souza MS, Rodrigues GZP, Petry IE, Andriguetti NB, Silva GJH, Gehlen G, da Silva LB (2017) Water quality parameters, biomarkers and metal bioaccumulation in native fish captured in the Ilha River, southern Brazil. Chemosphere 189:609–618
Dalzochio T, Rodrigues GZP, Simões LAR, Souza MS, Petry IE, Andriguetti NB, Silva GJH, Silva LB, Gehlen G (2018) In situ monitoring of the Sinos River, southern Brazil: water quality parameters, biomarkers, and metal bioaccumulation in fish. Environ Sci Pollut Res 25:9485–9500
Das RK, Nanda NK (1986) Induction of micronuclei in peripheral erythrocytes of fish Heteropneustes fossilis by mitomycin C and paper mill effluent. Mutat Res 175:67–71
Dashwood RH, Bailey GS (1998) Use of fish and fish transgenics in laboratory and field genotoxicology studies. Mutat Res 399:123–124
De Flora S, Bagnasco M, Zanacchi P (1991a) Genotoxic, carcinogenic, and teratogenic hazards in the marine environment, with special reference to the Mediterranean Sea. Mutat Res 258:285–320
De Flora S, Zanacchi P, Bagnasco M, Brunetti R, Majone F, Levis AG (1991b) Metabolic and genetic effects of marine pollution on aquatic organisms. In: Gledhill B, Mauro F (eds) Trends in biological dosimetry. Wiley-Liss, New York, pp 69–78
De Flora S, Viganò L, D’Agostini F, Camoirano A, Bagnasco M, Bennicelli C, Melodia F, Arillo A (1993) Multiple genotoxicity biomarkers in fish exposed in situ to polluted river water. Mutat Res 319:167–177
Deguchi Y, Toyoizumi T, Masuda S, Yasuhara A, Mohri S, Yamada M, Inoue Y, Kinae N (2007) Evaluation of mutagenic activities of leachates in landfill sites by micronucleus test and comet assay using goldfish. Mutat Res 627:178–185
Dertinger SD, Torous DK, Hayashi M, MacGregor JT (2011) Flow cytometric scoring of micronucleated erythrocytes: an efficient platform for assessing in vivo cytogenetic damage. Mutagenesis 26:139–145
Deutschmann B, Kolarevic S, Brack W, Kaisarevic S, Kostic J, Kracun-Kolarevic M, Liska I, Paunovic M, Seiler T-B, Shao Y, Sipos S, Slobodnik J, Teodorovic I, Vukovic-Gacic B, Hollert H (2016) Longitudinal profile of the genotoxic potential of the River Danube on erythrocytes of wild common bleak (Alburnus alburnus) assessed using the comet and micronucleus assay. Sci Total Environ 573:1441–1449
Dhawan A, Bajpayee M, Parmar D (2009) Comet assay: a reliable tool for the assessment of DNA damage in different models. Cell Biol Toxicol 25:5–32
Dixon DR, Pruski AM, Dixon LRJ, Jha AN (2002) Marine invertebrate eco-genotoxicology: a methodological overview. Mutagenesis 17:495–507
Dourado PLR, Rocha MP, Roveda LM, Raposo Junior JL, Cândido LS, Cardoso CAL, Morales MAM, Oliveira KMP, Grisolia AB (2017) Genotoxic and mutagenic effects of polluted surface water in the midwestern region of Brazil using animal and plant bioassays. Genet Mol Biol 40:123–133
Duarte IM, Dias MC, David JAO, Matsumoto ST (2012) A qualidade da água da Lagoa JacunĂ©m (EspĂrito Santo, Brasil) em relação a aspectos genotĂłxicos e mutagĂŞnicos, mensurados respectivamente pelo ensaio do cometa e teste do micronĂşcleo em peixes da espĂ©cie Oreochromis niloticus. R Bras Bioci 10:211–219 (in Portuguese)
Edwards JW, Edyvane KS, Boxall VA, Hamann M, Soole KL (2001) Metal levels in seston and marine fish flesh near industrial and metropolitan centres in South Australia. Mar Pollut Bull 42:389–396
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 20:320–328
Ergene S, Çavas T, Çelik A, Köleli N, Aymak C (2007a) Evaluation of river water genotoxicity using the piscine micronucleus test. Environ Mol Mutagen 48:421–429
Ergene S, Çavas T, Çelik A, Köleli N, Kaya F, Karahan A (2007b) Monitoring of nuclear abnormalities in peripheral erythrocytes of three fish species from the Goksu Delta (Turkey): genotoxic damage in relation to water pollution. Ecotoxicology 16:385–391
Escher BI, Leusch FDL (2012) Bioanalytical tools in water quality assessment. IWA Publishing, London
Escher BI, Neal PA, Leusch FDL (2015) Effect-based trigger values for in vitro bioassays: reading across from existing water quality guideline values. Water Res 81:137–148
Escher BI, Aїt-Aїssa S, Behnisch PA, Brack W, Brion F, Brouwer A, Buchinger S, Crawford SE, Du Pasquier D, Hamers T, Hettwer K, Hilscherová K, Hollert H, Kase R, Kienle C, Tindall AJ, Tuerk J, van der Oost R, Vermeirssen E, Neale PA (2018) Effect-based trigger values for in vitro and in vivo bioassays performed on surface water extracts supporting the environmental quality standards (EQS) of the European water framework directive. Sci Total Environ 628–629:748–765
European Community Marine Strategy Framework Directive (2008) Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). OJUnion, 1.164/19
European Union Water Framework Directive (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. OJEC 327:1–72
Falfushynska H, Horyn O, Fedoruk O, Khoma V, Rzymski P (2019) Difference in biochemical markers in the gibel carp (Carassius auratus gibelio) upstream and downstream of the hydropower plant. Environ Pollut 255:113213
Farag MR, Alagawany M (2018) Erythrocytes as a biological model for screening of xenobiotics toxicity. Chem Biol Interact 279:73–83
Fasulo S, Marino S, Mauceri A, Maisano M, Giannetto A, D’Agata A, Parrino V, Minutoli R, De Domenico E (2010) A multibiomarker approach in Coris julis living in a natural environment. Ecotoxicol Environ Saf 73:1565–1573
Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455:81–95
Fenech M, Chang WP, Kirsch-Volders M, Holland N, Bonassi S, Zeiger E, Human MicroNucleus Project (2003) HUMN project: detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutat Res 534:65–75
Fenech M, Kirsch-Volders M, Natarajan AT, Surralles J, Crott JW, Parry J, Norppa H, Eastmond DA, Tucker JD, Thomas P (2011) Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 26:125–132
Fernandez WS, Dias JF, Ribeiro CAO, Azevedo JS (2011) Liver damages and nuclear abnormalities in erythrocytes of Atherinella brasiliensis (Actynopterigii, Atherinopsidade) from two beaches in southeast of Brazil. Braz J Med Biol Res 59:163–169
Feron VJ, Schwarz M, Hemminki K, Krewski D (1999) Long- and medium-term carcinogenicity studies in animals and short-term genotoxicity tests. In: Moolgavkar S, Krewski D, Zeise L, Cardis E, Moller H (eds) Quantitative estimation and prediction of human cancer risks. IARC scientific publications n. 131. IARC, Lyon, pp 103–129
Ferreira GR, Nepomuceno JC (2008) Poluição do Rio Santa Catarina no Municipio de Vazante (MG) detectada por meio do teste do micronùcleo em peixes. Perquirēre 5:277–284 (in Portuguese)
Floehr T, Scholz-Starke B, Xiao H, Koch J, Wu L, Hou J, Wolf A, Bergmann A, Bluhm K, Yuan X, Roß-Nickoll M, Schäffer A, Hollert H (2015) Yangtze Three Gorges Reservoir, China: a holistic assessment of organic pollution, mutagenic effects of sediments and genotoxic impacts on fish. J Environ Sci 38:63–82
Flores-Galván MA, DaesslĂ© LW, Arellano-GarcĂa E, Torres-BugarĂn O, MacĂas-Zamora JV, Ruiz-Campos G (2020) Genotoxicity in fishes environmentally exposed to As, Se, Hg, Pb, Cr and toxaphene in the lower Colorado River basin, at Mexicali valley, Baja California, MĂ©xico. Ecotoxicology 29:493–502
Francisco CM, Bertolino SM, De Oliveira Júnior RJ, Morelli S, Pereira BB (2019) Genotoxicity assessment of polluted urban streams using a native fish Astyanax altiparanae. J Toxicol Environ Health A 82:514–523
Freire CA, Souza-Bastos LR, Chiesse J, Tincani FH, Piancini LDS, Randi MAF, Prodocimo V, Cestari MM, Assis HCS, Abilhoa V, Vitule JRS, Bastos LP, Oliveira-Ribeiro CA (2015) A multibiomarker evaluation of urban, industrial, and agricultural exposure of small characins in a large freshwater basin in southern Brazil. Environ Sci Pollut Res 22:13263–13277
Freire MM, Amorim LMF, Buch AC, Gonçalves AD, Sella SM, Cassella RJ, Moreira JC, Silva-Filho EV (2020) Polycyclic aromatic hydrocarbons in bays of the Rio de Janeiro state coast, SE – Brazil: effects on catfishes. Environ Res 181:108959
Frenzilli G, Falleni A, Scarcelli V, Del Barga I, Pellegrini S, Savarino G, Mariotti V, Benedetti M, Fattorini D, Regoli D, Nigro M (2008) Cellular responses in the cyprinid Leuciscus cephalus from a contaminated freshwater ecosystem. Aquat Toxicol 89:188–196
Frenzilli G, Nigro M, Lyons BP (2009) The comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat Res 681:80–92
Furnus GNA, Caffetti JD, Garcìa EM, Benìtez MF, Pastori MC, Fenocchio AS (2014) Baseline micronuclei and nuclear abnormalities frequencies in native fishes from the Paranà River (Argentina). Braz J Biol 74:217–221
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 Saf 98:103–109
Gajski G, Žegura B, Ladeira C, Novak M, Sramkova M, Pourrut B, Del Bo' C, Milić M, Gutzkow KB, Costa S, Dusinska M, Brunborg G, Collins A (2019) The comet assay in animal models: from bugs to whales – (part 2 vertebrates). Mutat Res 781:130–164
Galindo TP, Moreira LM (2009) Evaluation of genotoxicity using the micronucleus assay and nuclear abnormalities in the tropical sea fish Bathygobius soporator (Valenciennes, 1837) (Teleostei, Gobiidae). Genet Mol Biol 32:394–398
Gallão M, Gnocchi KG, Carvalho LR, Silva BF, Barbosa AN, Chippari-Gomes AT (2019) The impact of sublethal concentrations of treated leachate on Nile tilápia (Oreochromis niloticus). Bull Environ Contam Toxicol 102:519–524
Ghisi NC, Oliveira EC (2013) Evidence of contamination in the main body of the public water supply of Campo Mourão-PR: an analysis from a bioindicator of environmental quality. SaBios-Rev Saúde Biol 8:13–22
Ghisi NC, Oliveira EC, Fávaro LF, Assis HCS, Prioli AJ (2014) In situ assessment of a neotropical fish to evaluate pollution in a river receiving agricultural and urban wastewater. Bull Environ Contam Toxicol 93:699–709
Ghisi NC, Oliveira EC, Mota TFM, Vanzetto GV, Roque AA, Godinho JP, Bettim FL, Assis HCS, Prioli AJ (2016) Integrated biomarker response in catfish Hypostomus ancistroides by multivariate analysis in the Pirapó River, southern Brazil. Chemosphere 161:69–79
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 79:659–664
Gomes-Silva G, Pereira BB, Liu K, Chen B, Santos VSV, de Menezes GHT, Pires LP, Santos BMT, Oliveira DM, Machado PHA, de Oliveira JĂşnior RJ, de Oliveira AMM, Plath M (2020) Using native and invasive livebearing fishes (Poeciliidae, Teleostei) for the integrated biological assessment of pollution in urban streams. Sci Total Environ 698:134336
Gorbi S, Benedetti M, Virno Lamberti C, Pisanelli B, Moltedo G, Regoli F (2009) Biological effects of diethylene glycol (DEG) and produced waters (PWs) released from offshore activities: a multi-biomarker approach with the sea bass Dicentrarchus labrax. Environ Pollut 157:3166–3173
Gravato C, Santos MA (2002) Juvenile sea bass liver biotransformation and erythrocytic genotoxic responses to pulp mill contaminants. Ecotoxicol Environ Saf 53:104–112
Gravato C, Santos MA (2003) Dicentrarchus labrax biotransformation and genotoxicity responses after exposure to a secondary treated industrial/urban effluent. Ecotoxicol Environ Saf 55:300–306
Gravato C, Santos MA, Magalhães I (2000) Juvenile Dicentrarchus labrax L. biochemical and genotoxical responses after short-term exposure to ß-naphtoflavone and contaminated harbour waters. Fresenius Environ Bull 9:269–274
Grisolia CK, Starling FLRM (2001) Micronuclei monitoring of fishes from Lake Paranoá, under influence of sewage treatment plant discharges. Mutat Res 491:39–44
Grisolia CK, Oliveira ABB, Bonfim H, Klautau-Guimarães MN (2005) Genotoxicity evaluation of domestic sewage in a municipal wastewater treatment plant. Genet Mol Biol 28:334–338
Grisolia CK, Rivero CLG, Starling FLRM, da 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 32:138–143
Guilherme S, Válega M, Pereira ME, Santos MA, Pacheco M (2008) Erythrocytic nuclear abnormalities in wild and caged fish (Liza aurata) along an environmental mercury contamination gradient. Ecotoxicol Environ Saf 70:411–421
Gusso-Choueri PK, Choueri RB, Santos GS, Araújo GS, Cruz ACF, Stremel T, Campos SX, Cestari MM, Ribeiro CAO, Abessa DMS (2016) Assessing genotoxic effects in fish from a marine protected area influenced by former mining activities and other stressors. Mar Pollut Bull 104:229–239
Gutiérrez JM, Villar S, Plavan AA (2015) Micronucleus test in fishes as indicators of environmental quality in subestuaries of the Rìo de la Plata (Uruguay). Mar Pollut Bull 91:518–523
Hafez AM (2009) Mugil cephalus genome: a sensitive monitor for genotoxicity and cytotoxicity in aquatic environment. Aust J Basic Appl Sci 3:2176–2187
Hamann M, Boxall VA, Edyvane KS, Edwards JW, Soole KL (1999) Biochemical and cytogenetic biomarkers of pollutant exposure in marine fish (Aldrichetta forsteri Valenciennes and Sillago schomburgkii Peters) near industrial and metropolitan centres in South Australia. Biomarkers 4:290–302
Han Y, Li N, Oda Y, Ma M, Rao K, Wang Z, Jin W, Hong G, Li Z, Luo Y (2016) Evaluation of genotoxic effects of surface waters using a battery of bioassays indicating different mode of action. Ecotoxicol Environ Saf 133:448–456
Hansson T, Baršienė J, Tjärnlund U, Åkerman G, Linderoth M, Zebühr Y, Sternbeck J, Järnberg U, Balk L (2014) Cytological and biochemical biomarkers in adult female perch (Perca fluviatilis) in a chronically polluted gradient in the Stockholm recipient (Sweden). Mar Pollut Bull 81:27–40
Hariri M, Mirvaghefi A, Farahmand H, Taghavi L, Shahabinia A-R (2018) In situ assessment of Karaj River genotoxic impact with the alkaline comet assay and micronucleus test, on feral brown trout (Salmo trutta fario). Environ Toxicol Pharmacol 58:59–69
Hawkins WE, Overstreet RM, Walker WW (1988) Small fish models for identifying carcinogens in the aqueous environment. Water Res Bull 24:941–949
Hayashi M (2016) The micronucleus test – Most widely used in vivo genotoxicity test. Genes Environ 38:18
Hayashi M, Sofuni T, Ishidate M (1983) An application of acridine orange fluorescent staining to the micronucleus test. Mutat Res 120:241–247
Hayashi M, Ueda T, Uyeno K, Wada K, Kinae N, Saotome K, Tanaka N, Takai A, Sasaki YF, Asano N, Sofuni T, Ojima Y (1998) Development of genotoxicity assay systems that use aquatic organisms. Mutat Res 399:125–133
Hemachandra CK, Pathiratne A (2016) Combination of physico-chemical analysis, Allium cepa test system and Oreochromis niloticus erythrocyte based comet assay/nuclear abnormalities tests for cyto-genotoxicity assessments of treated effluents discharged from textile industries. Ecotoxicol Environ Saf 131:54–64
Hemachandra CK, Pathiratne A (2017) Cytogenotoxicity screening of source water, wastewater and treated water of drinking water treatment plants using two in vivo test systems: Allium cepa root based and Nile tilapia erythrocyte based tests. Water Res 108:320–329
Hooftman RN, de Raat WK (1982) Induction of nuclear anomalies (micronuclei) in the peripheral blood erythrocytes of the eastern mudminnow Umbra pygmea by ethyl methanesulphonate. Mutat Res 104:147–152
Hooftman RN, Vink GJ (1981) Cytogenetic effects on the eastern mudminnow Umbra pygmea exposed to ethyl methanesulphonate, benzo[a]pyrene, and river water. Ecotoxicol Environ Saf 5:261–269
Hook SE, Gallagher EP, Batley GE (2014) The role of biomarkers in the assessment of aquatic ecosystem health. Integr Environ Assess Manag 10:327–341
Hose JE (1994) Large-scale genotoxicity assessments in the marine environment. Environ Health Perspect 102(Suppl. 12):29–32
Hose JE, Cross JN, Smith SG, Diehl D (1987) Elevated circulating erythrocyte micronuclei in fishes from contaminated sites of Southern California. Mar Environ Res 22:167–176
Hoshina MM, de Franceschi de Angelis D, Marin-Morales MA (2008) Induction of micronucleus and nuclear alterations in fish (Oreochromis niloticus) by a petroleum refinery effluent. Mutat Res 656:44–48
Houk VS (1992) The genotoxicity of industrial wastes and effluents. A review. Mutat Res 277:91–138
Hughes JB, Hebert AT (1991) Erythrocyte micronuclei in winter flounder (Pseudopleuronectes americanus): results of field surveys during 1980-1988 from Virginia to Nova Scotia and in Long Island sound. Arch Environ Contam Toxicol 20:474–479
Hurtado-AlarcĂłn JC, Solarte-David VA, LĂłpez-Ortiz JB, Montoya-Herrera FL (2007) Prueba de micronĂşcleos en eritrocitos de sabaletas (Brycon henni E.) presentes en el rĂo Porce y en el Embalse Porce II, Antioquia. Revista ElectrĂłn Ing Prod AcuĂcola 2:238–245 (in Spanish)
Hussain B, Sultana T, Sultana S, Masoud MS, Ahmed Z, Mahboob S (2018) Fish eco-genotoxicology: comet and micronucleus assay in fish erythrocytes as in situ biomarker of freshwater pollution. Saudi J Biol Sci 25:393–398
Hussain B, Fatima M, Al-Ghanim KA, Al-Misned F, Mahboob S (2020) Assessment of DNA integrity through MN bioassay of erythrocytes and histopathological changes in Wallago attu and Cirrhinus mirigala in response to freshwater pollution. Saudi J Biol Sci 27:251–260
Ilyinskikh NN, Ilyinskikh EN, Ilyinskikh IN (1998) Micronucleated erythrocytes frequency and radiocesium bioconcentration in pikes (Esox lucius) caught in the Tom River near the nuclear facilities of the Siberian Chemical Complex (Tomsk-7). Mutat Res 421:197–203
Ivanova L, Popovska-Percinic F, Slavevska-Stamenkovic V, Jordanova M, Rebok K (2016) Micronuclei and nuclear abnormalities in erythrocytes from barbel Barbus Peloponnesius revealing genotoxic pollution of the river Bregalnica. Maced Vet Rev 39:159–166
Jesus IS, Cestari MM, Bezerra MA, Affonso PRAM (2016) Genotoxicity effects in freshwater fish from a brazilian impacted river. Bull Environ Contam Toxicol 96:490–495
Jha AN (2004) Genotoxicological studies in aquatic organisms: an overview. Mutat Res 552:1–17
Jovanović J, Kolarević S, Milošković A, Radojković N, Simić V, Dojčinović B, Kračun-Kolarević M, Paunović M, Kostić J, Sunjog K, Timilijić J, Djordjević J, Gačić Z, Žegura B, Vuković-Gačić B (2018) Evaluation of genotoxic potential in the Velika Morava River Basin in vitro and in situ. Sci Total Environ 621:1289–1299
Kanev MO, Ozdemir K, Muranli FDG (2016) Genotoxic evaluation of the Ergene River, Turkey, on mosquito fish, Gambussia affinis (Baird and Girard, 1853) using the piscine micronucleus assay. Int J Aquat Biol 4:330–339
Katsumiti A, Valdez Domingos FX, Azevedo M, Silva MD, Damian RC, Almeida MIM, Silva de Assis HC, Cestari MM, Randi MAF, Oliveira Ribeiro CA, Freire CA (2009) An assessment of acute biomarker responses in the demersal catfish Cathorops spixii after the Vicuña Oil Spill in a harbour estuarine area in Southern Brazil. Environ Monit Assess 152:209–222
Kienzler A, Bopp SK, van der Linden S, Berggren E, Worth A (2016) Regulatory assessment of chemical mixtures: requirements, current approaches and future perspectives. Regul Toxicol Pharmacol 80:321–334
Kirschbaum AA, Seriani R, Pereira CDS, Assunção A, Abessa DMS, Rotundo MM, Ranzani-Paiva MJT (2009) Cytogenotoxicity biomarkers in fat snook Centropomus parallelus from Cananéia and São Vicente estuaries, SP, Brazil. Genet Mol Biol 32:151–154
Kligerman AD (1982) Fishes as biological detectors of the effects of genotoxic agents. In: Heddle JA (ed) Mutagenicity: new horizons in genetic toxicology. Academic, New York, pp 435–453
Kligerman AD, Bloom S (1975) A cytogenetics model for the study of chromosome aberrations in fishes. Mutat Res 31:334–335a
Kligerman AD, Bloom SE, Howell WM (1975) Umbra limi: a model for the study of chromosomes aberrations in fishes. Mutat Res 31:225–233
Klobučar GI, Stambuk A, Pavlica M, Peric MS, Hackenberger BK, Hylland K (2010) Genotoxicity monitoring of freshwater environments using caged carp (Cyprinus carpio). Ecotoxicology 19:77–84
Klymenko MO, Biedunkova OO (2016) Development stability and cytogenetic homeostasis of Perca fluviatilis (Percifomes, Percidae) in the rivers of Rivne Region. Vestn Zool 50:539–546
Klymenko MO, Biedunkova OO, Klymenko OM, Statnyk II (2018) Influence of river water quality on homeostasis characteristics of cypriniform and perciform fish. Biosyst Divers 26:16–23
KnasmĂĽller S, Fenech M (2019) The micronucleus assay in toxicology. Issues in toxicology. The Royal Society of Chemistry, Cambridge
Koca S, Koca YB, Yildiz S, Gürcü B (2008) Genotoxic and histopathological effects of water pollution on two fish species, Barbus capito pectoralis and Chondrostoma nasus in the Büyük Menderes River, Turkey. Biol Trace Elem Res 122:276–291
Köhler A, Ellesat K (2008) Nuclear changes in blood, early liver anomalies and hepatocellular cancers in flounder (Platichthys flesus L.) as prognostic indicator for a higher cancer risk? Mar Environ Res 66:149–150
Kolak A, Treer T, Anicic I, Safner R (1999) Monitoring the genotoxicity of the river Sava by micronuclei in chub (Leuciscus cephalus). Cytobios 392:135–142
Kolarević S, Aborgiba M, Kračun-Kolarević M, Kostić J, Simonović P, Simić V, Milošković A, Reischer G, Farnleitner A, Gačić Z, Milačič R, Zuliani T, Vidmar J, Pergal M, Piria M, Paunović M, Vuković-Gačić B (2016) Evaluation of genotoxic pressure along the Sava river. PLoS One 11:e0162450
Kontaş S, Bostancı D (2020) Genotoxic effects of environmental pollutant heavy metals on Alburnus chalcoides (Pisces: Cyprinidae) inhabiting lower Melet River (Ordu, Turkey). Bull Environ Contam Toxicol 104:763–769
Kopecka J, Lehtonen KK, Barsiene J, Broeg K, Vuorinen PJ, Gercken J, Pempkowiak J (2006) Measurements of biomarker levels in flounder (Platichthys flesus) and blue mussel (Mytilus trossulus) from the Gulf of Gdansk (Southern Baltic). Mar Poll Bull 53:406–421
Kračun-Kolarević M, Kolarević S, Jovanović J, Marković V, Ilić M, Simonović P, Simić V, Gačić Z, Diamantini E, Stella E, Petrović M, Majone B, Bellin A, Paunović M, Vuković-Gačić B (2016) Evaluation of genotoxic potential throughout the upper and middle stretches of Adige river basin. Sci Total Environ 571:1383–1391
Kroon F, Streten C, Harries S (2017) A protocol for identifying suitable biomarkers to assess fish health: a systematic review. PLoS One 12:e0174762
Kushwaha B, Pandey S, Sharma S, Srivastava R, Kumar R, Nagpure NS, Dabas A, Srivastava SK (2012) In situ assessment of genotoxic and mutagenic potential of polluted river water in Channa punctatus and Mystus vittatus. Int Aquat Res 4:16
Lacerda D, Vergilio CS, Silva Souza T, Costa LHV, Rangel TP, Oliveira BCV, Almeida DQR, Pestana IA, Almeida MG, Rezende CE (2020) Comparative metal accumulation and toxicogenetic damage induction in three neotropical fish species with distinct foraging habits and feeding preferences. Ecotoxicol Environ Saf 195:110449
Lapuente J, Lourenço J, Mendo SA, Borràs M, Martins MG, Costa PM, Pacheco M (2015) The Comet assay and its applications in the field of ecotoxicology: a mature tool that continues to expand its perspectives. Front Genet 6:180
Lasheen MR, Abdel-Gawad FK, Alaneny AA, Abd El Bary HMH (2012) Fish as bioindicators in aquatic environmental pollution assessment: a case study in Abu-Rawash area, Egypt. World Appl Sci J 19:265–275
Lee RF, Steinert S (2003) Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat Res 544:43–64
Lehtonen KK, Schiedek D, Köhler A, Lang T, Vuorinen PJ, Förlin L, Baršienė J, Pempkowiak J, Gercken J (2006) The BEEP project in the Baltic Sea: overview of results and outline for a regional biological effects monitoring strategy. Mar Poll Bull 53:523–537
Lemos CT, Rödel PM, Terra NR, Oliveira NCD, Erdtmann B (2007) River water genotoxicity evaluation using micronucleus assay in fish erythrocytes. Ecotoxicol Environ Saf 66:391–401
Lemos CT, Almeida Iranco F, 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 406:337–343
Leusch FDL, Snyder SA (2015) Bioanalytical tools: half a century of application for potable reuse. Environ Sci Water Res Technol 1:606–621
Lima Cardoso R, Carvalho-Neta RNF, Castro ACL, Ferreira CFC, Silva MHL, Jesus Azevedo JW, Sobrinho JRSC, Santos DMS (2018) Histological and genotoxic biomarkers in Prochilodus lacustris (Pisces, Prochilodontidae) for environmental assessment in a protected area in the Northeast of Brazil. Bull Environ Contam Toxicol 101:570–579
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 237:611–624
Lima ARB, Torres RA, Jacobina UP, Pinheiro MAA, Adam ML (2019) Genomic damage in Mugil curema (Actinopterygii: Mugilidae) reveals the effects of intense urbanization on estuaries in northeastern Brazil. Mar Poll Bull 138:63–69
Lindberg HK, Wang X, Järventaus H, Falck GC-M, Norppa H, Fenech M (2007) Origin of nuclear buds and micronuclei in normal and folate-deprived human lymphocytes. Mutat Res 617:33–45
Linde-Arias AR, Inácio AF, Alburquerque 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 399:186–192
Liney K, Hagger JA, Tyler CR, Depledge MH, Galloway TS, Jobling S (2006) Health effects in fish of long-term exposure to effluents from wastewater treatment works. Environ Health Perspect 114(Suppl. 1):81–89
Llorente MT, Martos A, Castaño A (2002) Detection of cytogenetic alterations and blood cell changes in natural populations of carp. Ecotoxicology 11:27–34
Long ER, Buchman MF (1989) An evaluation of candidate measures of biological effects for the national status and trends program. NOAA Tech. Memo., NOS OMA 45
Longwell AC, Perry D, Hughes JB, Hebert A (1983) Frequencies of micronuclei in mature and immature erythrocytes of fish as an estimate of chromosome mutation rates-results of field surveys on windowpane flounder, winter flounder and Atlantic mackerel. International Council for the Exploration of the Sea, C.M. 1983/E:55, Marine Environmental Quality Committee, Ref. Demersal and Pelagic Fish Committees, 14 pp
Longwell AC, Chang S, Hebert A, Hughes JB, Perry D (1992) Pollution and developmental abnormalities in Atlantic fishes. Environ Biol Fish 35:1–21
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 13:569–578
Lugas’kova NV (2003) Species specificity of the cytogenetic stability of fish in a eutrophic water body. Russ J Ecol 34:210–214
Luzhna L, Kathiria P, Kovalchuk O (2013) Micronuclei in genotoxicity assessment: from genetics to epigenetics and beyond. Front Genet 4:131
Lyne TB, Bickham JW, Lamb T, Gibbons JW (1992) The application of bioassays in risk assessment of environmental pollution. Risk Anal 12:361–365
Maceda-Veiga A, Monroy M, Viscor G, De Sostoa A (2010) Changes in non-specific biomarkers in the Mediterranean barbel (Barbus meridionalis) exposed to sewage effluents in a Mediterranean stream (Catalonia, NE Spain). Aquat Toxicol 100:229–237
Maceda-Veiga A, Monroy M, Navarro E, Viscor G, De Sostoa A (2013) Metal concentrations and pathological responses of wild native fish exposed to sewage discharge in a Mediterranean river. Sci Total Environ 449:9–19
MacGregor JT, Wehr CM, Gould DH (1980) Clastogen-induced micronuclei in peripheral blood erythrocytes: the basis of an improved micronucleus test. Environ Mutagen 2:509–514
Mallick P, Khuda-Bukhsh AR (2003) Nuclear anomalies and blood protein variations in fish of the Hooghly-Matlah River system, India, as an indicator of genotoxicity in water. Bull Environ Contam Toxicol 70:1071–1082
Manna GK, Banerjee G, Gupta S (1985) Micronuclei test in the peripheral erythrocytes of the exotic fish, Oreochromis massambica. Nucleus 28:176–179
Maria VL, Correia AC, Santos MA (2003a) Genotoxic and hepatic biotransformation responses induced by the overflow of pulp mill and secondary-treated effluents on Anguilla anguilla L. Ecotoxicol Environ Saf 55:126–137
Maria VL, Correia AC, Santos MA (2003b) Genotoxic and biochemical responses in caged eel (Anguilla anguilla L.) after short-term exposure to harbour waters. Environ Int 29:923–929
Maria VL, Teles M, Pacheco M, Correia AC, Santos MA (2004) Biomarker responses in a polluted river: effects of pulp and paper mill contaminants on caged Anguilla anguilla L. Fresenius Environ Bull 13:317–325
Marlasca MJ, Sanpera C, Riva MC, Sala R, Crespo S (1998) Hepatic alterations and induction of micronuclei in rainbow trout (Oncorhynchus mykiss) exposed to a textile industry effluent. Histol Histopathol 13:703–712
Matsumoto ST, Mantovani MS, Malaguttii MIA, Dias AL, Fonseca IC, Marin-Morales MA (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 29:148–158
McGregor DB, Rice JM, Venitt S (1999) The use of short- and medium-term tests for carcinogens and data on genetic effects in carcinogenic hazard evaluation. IARC scientific publications, vol. 146. IARC, Lyon
Melo KM, Alves IR, Pieczarka JC, Oliveira David JA, Nagamachi CY, Grisolia CK (2013) Profile of micronucleus frequencies and nuclear abnormalities in different species of electric fishes (Gymnotiformes) from the Eastern Amazon. Genet Mol Biol 36:425–429
Metcalfe CD (1988) Induction of micronuclei and nuclear abnormalities in the erythrocytes of mudminnows (Umbra limi) and brown bullheads (Ictalurus nebulosus). Bull Environ Contam Toxicol 40:489–495
Meyer JN (2010) QPCR: a tool for analysis of mitochondrial and nuclear DNA damage in ecotoxicology. Ecotoxicology 19:804–811
Mijat V (2005) Micronucleus test in most recent ichthiology research. Ribarstvo 63:21–32 (in Serbian)
Minissi S, Ciccotti E, Rizzoni M (1996) Micronucleus test in erythrocytes of Barbus plebejus (Teleostei, Pisces) from two natural environments: a bioassay for the in situ detection of mutagens in freshwater. Mutat Res 367:245–251
Mitchelmore CL, Chipman JK (1998) DNA strand breakage in aquatic organisms and the potential value of the comet assay in environmental monitoring. Mutat Res 399:135–147
Mohmood I, Maria VL, Oliveira M, Ahmad I, Pacheco M, Santos MA (2008) Seasonal assessment of a contaminated coastal lagoon (Ria de Aveiro, Portugal) using Dicentrarchus labrax L. erythrocytic nuclear abnormalities. Fresenius Environ Bull 17:1924–1931
Monserrat JM, MartĂnez PE, Geracitano LA, Amado LL, Martins CM, Pinho GL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C Toxicol Pharmacol 146:221–234
Montesano R, Bartsch R, Vainio H, Wilbourn J, Yamasaki H (1987) Long-term and short-term assays for carcinogens. A critical appraisal. IARC scientific publications, vol. 83. IARC, Lyon
Morais CR, Carvalho SM, Araujo GR, Souto HN, Bonetti AM, Morelli S, Campos Júnior EO (2016) Assessment of water quality and genotoxic impact by toxic metals in Geophagus brasiliensis. Chemosphere 152:328–334
Morina V, Aliko V, Gavazaj F, Kastrati D (2012) Use of blood parameters as biomarkers of contaminant exposure in fish specimens from Sitnica River, Kosovo. J Int Environ Appl Sci 7:971–977
Müller L (2009) In-vitro genotoxicity tests to detect carcinogenicity: a systematic review. Hum Exp Toxicol 28:131–133
Nagpure NS, Srivastava R, Kumar R, Dabas A, Kushwaha B, Kumar P (2015) Assessment of pollution of river Ganges by tannery effluents using genotoxicity biomarkers in murrel fish, Channa punctatus (Bloch). Indian J Exp Biol 53:476–483
Napierska D, Barsiene J, Mulkiewicz E, Podolska M, Rybakovas A (2009) Biomarker responses in flounder Platichthys flesus from the Polish coastal area of the Baltic Sea and applications in biomonitoring. Ecotoxicology 18:846–859
Obiakor MO, Ezeonyejiaku CD, Ezenwelu CO, Ugochukwu GC (2010) Aquatic genetic biomarkers of exposure and effect in catfish (Clarias gariepinus, Burchell, 1822). Am-Euras J Toxicol Sci 2:196–202
Obiakor MO, Okonkwo JC, Nnabude PC, Ezeonyejiaku CD (2012) Eco-genotoxicology: micronucleus assay in fish erythrocytes as in situ aquatic pollution biomarker. A review. J Anim Sci Adv 2:123–133
Obiakor MO, Okonkwo JC, Ezeonyejiaku CD (2014) Genotoxicity of freshwater ecosystem shows DNA damage in preponderant fish as validated by in vivo micronucleus induction in gill and kidney erythrocytes. Mutat Res 775–776:20–30
Odeigah PG, Osanyinpeju AO (1995) Genotoxic effects of two industrial effluents and ethyl methane sulfonate in Clarias lazera. Food Chem Toxicol 33:501–505
Ohe T, Watanabe T, Wakabayashi K (2004) Mutagens in surface waters: a review. Mutat Res 567:109–149
Oikari A (2006) Caging techniques for field exposure of fish to chemical contaminants. Aquat Toxicol 78:370–381
Ojima Y, Ueno K, Hayashi M (1976) A review of the chromosome number of fish. La Kromosomo 2:19–47
Okoye CN, Mac Donald-Jay N, Kamunde C (2019) Effects of bioenergetics, temperature and cadmium on liver mitochondria reactive oxygen species production and consumption. Aquat Toxicol 214:105264
Oliveira M, Ahmad I, Maria VL, Ferreira CSS, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2010a) Evaluation of oxidative DNA lesions in plasma and nuclear abnormalities in erythrocytes of wild fish (Liza aurata) as an integrated approach to genotoxicity assessment. Mutat Res 703:83–89
Oliveira M, Maria VL, Ahmad I, Teles M, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2010b) Golden grey mullet and sea bass oxidative DNA damage and clastogenic/aneugenic responses in a contaminated coastal lagoon. Ecotoxicol Environ Saf 73:1907–1913
Oliveira-Martins CR, Grisolia CK (2009) Toxicity and genotoxicity of wastewater from gasoline stations. Genet Mol Biol 32:853–856
Omar WA, Zaghloul KH, Abdel-Khalek AA, Abo-Hegab S (2012) Genotoxic effects of metal pollution in two fish species, Oreochromis niloticus and Mugil cephalus, from highly degraded aquatic habitats. Mutat Res 746:7–14
Osman AGM, Kloas W (2010) Water quality and heavy metal monitoring in water, sediments, and tissues of the African catfish Clarias gariepinus (Burchell, 1822) from the River Nile, Egypt. J Environ Prot 1:389–400
Osman AGM, Abd El Reheem AM, Moustafa MA, Mahmoud UM, Abuel-Fadl KY, Kloas W (2011) In situ evaluation of the genotoxic potential of the river Nile: I. Micronucleus and nuclear lesion tests of erythrocytes of Oreochromis niloticus niloticus (Linnaeus, 1758) and Clarias gariepinus (Burchell, 1822). Toxicol Environ Chem 93:1002–1017
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 Saf 133:73–81
Ossana NA, Baudou FG, Castañé PM, Tripoli L, Soloneski S, Ferrari L (2019) Histological, genotoxic, and biochemical effects on Cnesterodon decemmaculatus (Jenyns 1842) (Cyprinodontiformes, Poeciliidae): early response bioassays to assess the impact of receiving waters. J Toxicol 2019:4687685
Pacheco M, Santos MA (1996) Induction of micronuclei and nuclear abnormalities in the erythrocytes of Anguilla anguilla L. exposed either to cyclophosphamide or to bleached kraft pulp mill effluent. Fresenius Environ Bull 5:746–751
Pacheco M, Santos MA (1999) Biochemical and genotoxic responses of adult eel (Anguilla anguilla L.) to resin acids and pulp mill effluent: laboratory and field experiments. Ecotoxicol Environ Saf 42:81–93
Pacheco M, Santos MA (2001) Biotransformation, endocrine, and genetic responses of Anguilla anguilla L. to petroleum distillate products and environmentally contaminated waters. Ecotoxicol Environ Saf 49:64–75
Pacheco M, Santos MA, Teles M, Oliveira M, Rebelo JE, Pombo L (2005) Biotransformation and genotoxic biomarkers in mullet species (Liza sp.) from a contaminated coastal lagoon (Ria de Aveiro, Portugal). Environ Monit Assess 107:133–153
Palacio-Betancur I, Palacio-Baena JA, Camargo-Guerrero M (2009) Micronuclei test application to wild tropical ichthyic species common in two lentic environments of the low zones in Colombia. Actual Biol 31:67–77
Palm A, Krause T (1995) Micronucleated erythrocytes in fish from several Estonian waterbodies. Proc Estonian Acad Sci Biol 44:69–77
Palm A, Tuvikene A, Krause T (1992) Changes of hematological characteristics of the rainbow trout (Oncorhynchus mykiss) reared in the mixture of natural and oil-shale mine drainage water. Proc Estonian Acad Sci Biol 41:183–181
Pampanin DM, Brooks SJ, Grøsvik BE, Le Goff J, Meier S, Sydnes MO (2017) DNA adducts in marine fish as biological marker of genotoxicity in environmental monitoring: the way forward. Mar Environ Res 125:49–62
Pantaleão SM, Alcântara AV, Alves JPH, Spanó MA (2006) The piscine micronucleus test to assess the impact of pollution on the Japaratuba river in Brazil. Environ Mol Mutagen 47:219–224
Pavlica M, Stambuk A, Malovic L, Mladinic M, Klobucar GI (2011) DNA integrity of chub erythrocytes (Squalius cephalus L.) as an indicator of pollution-related genotoxicity in the river Sava. Environ Monit Assess 177:85–94
Pimenta VMSD, Silva JM, Nepomuceno JC, Pavanin LA (2013) In situ assessment of the Paraguay River water, in Brazilian Pantanal, by means of micronucleus assay with fish and chemical analysis. Bull Environ Contam Toxicol 90:427–433
Pinheiro-Sousa DB, Torres Junior AR, Silva D, Santos RL, Carvalho Neta RNF (2019) A screening test based on hematological and histological biomarkers to evaluate the environmental impacts in tambaqui (Colossoma macropomum) from a protected area in Maranhão, Brazilian Amazon. Chemosphere 214:445–451
Polard T, Jean S, Gauthier L, Laplanche C, Merlina G, Sánchez-Pérez JM, Pinelli E (2011a) Mutagenic impact on fish of runoff events in agricultural areas in south-west France. Aquat Toxicol 101:126–134
Polard T, Jean S, Merlina G, Laplanche C, Pinelli E, Gauthier L (2011b) Giemsa versus acridine orange staining in the fish micronucleus assay and validation for use in water quality monitoring. Ecotoxicol Environ Saf 74:144–149
Poongothai K, Shayin S, Usharani MV (1996) Induction of micronuclei in fish by polluted water and heavy metal. Cytobios 86:17–22
Porto JIR, Araujo CSO, Feldberg E (2005) Mutagenic effects of mercury pollution as revealed by micronucleus test on three Amazonian fish species. Environ Res 97:287–292
Powers DA (1989) Fish as model systems. Science 246:352–358
Prasse C, Stalter D, Schulte-Oehlmann U, Oehlmann J (2015) Spoilt for choice: a critical review on the chemical and biological assessment of current wastewater treatment technologies. Water Res 87:237–270
Praveena M, Sailaja MC, Rao KJ (2014) Clastogenic effects induced due to chromium intoxication in a freshwater fish, Labeo rohita. Int J Adv Sci Tech Res 4:647–656
Ramsdorf WA, Vicari T, Almeida MIM, Artoni RF, Cestari MM (2012) Handling of Astyanax sp. for biomonitoring in Cangüiri Farm within a fountainhead (Iraà River Environment Preservation Area) through the use of genetic biomarkers. Environ Monit Assess 184:5841–5849
Rebok K, Jordanova M, Slavevska-Stamenković V, Ivanova L, Kostov V, Stafilov T, Rocha E (2017) Frequencies of erythrocyte nuclear abnormalities and of leucocytes in the fish Barbus peloponnesius correlate with a pollution gradient in the River Bregalnica (Macedonia). Environ Sci Pollut Res 24:10493–10509
Ribeiro DL, Barcelos GRM, Arce LPG (2014) Genotoxic effects of water from São Francisco River, Brazil, in Astyanax paranae. Bull Environ Contam Toxicol 93:274–279
Risjani Y, Loppion G, Couteau J, Yunianta Y, Widowati I, Hermawati A, Minier C (2020) Genotoxicity in the rivers from the Brantas catchment (East Java, Indonesia): occurrence in sediments and effects in Oreochromis niloticus (Linnæus 1758). Environ Sci Pollut Res 27:21905–21913
Rocha PS, Luvizotto GL, Kosmehl T, Böttcher M, Storch V, Braunbeck T, Hollert H (2009) Sediment genotoxicity in the Tiete River (São Paulo, Brazil): in vitro comet assay versus in situ micronucleus assay studies. Ecotoxicol Environ Saf 72:1842–1848
Rocha CAM, Pessoa CMF, Rodrigues CAC, Pinheiro RHS, Costa ET, Guimarães AC, Burbano RR (2016) Investigation into the cytotoxicity and mutagenicity of the Marajó archipelago waters using Plagioscion squamosissimus (Perciformes: Sciaenidae) as a bioindicator. Ecotoxicol Environ Saf 132:111–115
Rocha MP, Dourado PLR, Cardoso CAL, Cândido LS, Pereira JG, Oliveira KMP, Grisolia AB (2018) Tools for monitoring aquatic environments to identify anthropic effects. Environ Monit Assess 190:61–73
Rodriguez-Cea A, Ayllon F, Garcia-Vazquez E (2003) Micronucleus test in freshwater fish species: an evaluation of its sensitivity for application in field surveys. Ecotoxicol Environ Saf 56:442–448
Ross SW, Dalton DA, Kramer S, Christensen BL (2001) Physiological (antioxidant) responses of estuarine fishes to variability in dissolved oxygen. Comp Biochem Physiol C Toxicol Pharmacol 130:289–303
Russo C, Rocco L, Morescalchi MA, Stingo V (2004) Assessment of environmental stress by the micronucleus test and the comet assay on the genome of teleost populations from two natural environments. Ecotoxicol Environ Saf 57:168–174
Rybakovas A, Barsiene J, Lang T (2009) Environmental genotoxicity and cytotoxicity in the offshore zones of the Baltic and the north seas. Mar Environ Res 68:246–256
Salamone M, Heddle J, Stuart E, Katz M (1980) Towards an improved micronucleus test. Studies on 3 model agents, mitomycin C, cyclophosphamide and dimethylbenzanthracene. Mutat Res 74:347–356
Saleh KAJ (2010) The intensity of pollutant genotoxicity in Lake Uluabat. Int J Biotechnol Biochem 6:625–631
Saleh KAJ, Alshehri MA (2011) The intensity of pollutant genotoxicity in Lake Uluabat: investigation of the peripheral erythrocytes of Cyprinus carpio. Afr J Biotechnol 10:16045–16050
Salvagni J, Ternus RZ, Fuentefria AM (2011) Assessment of the genotoxic impact of pesticides on farming communities in the countryside of Santa Catarina State, Brazil. Genet Mol Biol 34:122–126
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
Sánchez-Galán S, Linde AR, Izquierdo JI, GarcĂa-Vázquez E (1998) Micronuclei and fluctuating asymmetry in brown trout (Salmo trutta): complementary methods to biomonitor freshwater ecosystems. Mutat Res 412:219–225
Sánchez-Galán S, Linde AR, Ayllon F, GarcĂa-Vázquez E (2001) Induction of micronuclei in eel (Anguilla anguilla L.) by heavy metals. Ecotoxicol Environ Saf 49:139–143
SanJuan-Reyes N, GĂłmez-Oliván LM, Galar-MartĂnez M, GarcĂa-Medina S, Islas-Flores H, González-González ED, Cardoso-Vera JD, JimĂ©nez-Vargas JM (2015) NSAID-manufacturing plant effluent induces geno- and cytotoxicity in common carp (Cyprinus carpio). Sci Total Environ 530–531:1–10
Schiedek D, Broeg K, Barsiene J, Lehtonen KK, Gercken J, Pfeifer S, Vuontisjärvi H, Vuorinen PJ, Dedonyte V, Koehler A, Balk L, Schneider R (2006) Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea. Mar Pollut Bull 53:387–405
Schlegel R, MacGregor JT (1982) The persistence of micronuclei in peripheral blood erythrocytes: detection of chronic chromosome breakage in mice. Mutat Res 104:367–369
Schlegel R, MacGregor JT (1983) A rapid screen for cumulative chromosome damage in mice. Accumulation of circulating micronucleated erythrocytes. Mutat Res 113:481–487
Schmid W (1975) The micronucleus test. Mutat Res 31:9–15
Schultz N, Norrgren L, Grawe J, Johannisson A, Medhage O (1993) Micronuclei frequency in circulating erythrocytes from rainbow trout (Oncorhynchus mykiss) subjected to radiation, an image analysis and flow cytometric study. Comp Biochem Physiol C 105:207–211
Seriani R, Ranzani-Paiva MJT, Silva-Souza AT, Napoleão SR (2011) Hematology, micronuclei and nuclear abnormalities in fishes from São Francisco river, Minas Gerais state, Brazil. Acta Sci Biol Sciences 33:107–112
Seriani R, Abessa DMS, Kirschbaum AA, Pereira CDS, Ranzani-Paiva MJT, Assunçao A, Silveira FL, Romano P, Mucci JLN (2012) Water toxicity and cyto-genotoxicity biomarkers in the fish Oreochromis niloticus (Cichlidae). J Braz Soc Ecotoxicol 7:67–72
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 Saf 112:162–168
Serrano-Garcìa L, Montero-Montoya R (2001) Micronuclei and chromatin buds are the result of related genotoxic events. Environ Mol Mutagen 38:38–45
Silva Souza T, Fontanetti CS (2006) Micronucleus test and observation of nuclear alterations in erythrocytes of Nile tilapia exposed to waters affected by refinery effluent. Mutat Res 605:87–93
Silva MD, Rossi SC, Ghisi NC, Ribeiro CAO, Cestari MM, Assis HCS (2014) Using multibiomarker approach as a tool to improve the management plan for a Private Reserve of Natural Heritage (RPPN). Bull Environ Contam Toxicol 92:602–608
Silva EB, Corrêa SAS, Abessa DMS, Silva BFX, Rivero DHRF, Seriani R (2018) Mucociliary transport, differential white blood cells, and cyto-genotoxicity in peripheral erythrocytes in fish from a polluted urban pond. Environ Sci Pollut Res 25:2683–2690
Smagin AI, Lugaskova NV, Menshikh TB (2005) Study of fish from the Techa river waste storage reservoir with micronuclei testing method. Izv Chelyabinskogo nauchnogo tsentra UrO RAN 1:105–109 (in Russian)
Smith IR (1990) Erythrocytic micronuclei in wild fish from Lakes Superior and Ontario that have pollution-associated neoplasia. J Great Lakes Res 16:139–142
Soldatov AA (1995) Peculiarities of organization and functioning of the fish red blood system. J Evol Biochem Physiol 41:272–281
Sommer S, Buraczewska I, Kruszewski M (2020) Micronucleus assay: the state of art, and future directions. Int J Mol Sci 21:1534
Sousa EL, Pereira NJ, Gomes JB, Santos MM, Santos DMS (2020) Ecotoxicological analyses of springs of a Brazilian Northeast Conservation Unit. Bull Environ Contam Toxicol 104:27–34
Souza IC, Duarte ID, Pimentel NQ, Rocha LD, Morozesk M, Bonomo MM, Azevedo VC, Pereira CDS, Monferrán MV, Milanez CRD, Matsumoto ST, Wunderlin DA, Fernandes MN (2013) Matching metal pollution with bioavailability, bioaccumulation and biomarkers response in fish (Centropomus parallelus) resident in neotropical estuaries. Environ Pollut 180:136–144
Spies RB, Stegeman JJ, Rice DW, Woodlin B, Thomas P, Hose JE, Cross JN, Prieto M (1990) Sublethal responses of Platichtus stellatus to organic contamination in San Francisco Bay with emphasis on reproduction. In: McCarthy JF, Shugart LR (eds) Biomarkers of environmental contamination. CRC Press, Boca Raton, pp 87–122
Sposito JCV, Francisco LFV, Crispim BA, Silva Dantas FG, Souza JP, Viana LF, Solórzano JCJ, Oliveira KMP, Barufatti A (2019) Influence of land use and cover on toxicogenetic potential of surface water from Central-West Brazilian rivers. Arch Environ Contam Toxicol 76:483–495
Šrut M, Stambuk A, Pavlica M, Klobucar GI (2010) Cage exposure of european sea bass (Dicentrarchus labrax) for in situ assessment of pollution-related genotoxicity. Arh Hig Rada Toksikol 61:29–36
Stahl RGJ (1991) The genetic toxicology of organic compounds in natural waters and waste waters. Ecotoxicol Environ Saf 22:94–125
Stegeman JJ, Lech JJ (1991) Cytochrome P-450 monooxygenase systems in aquatic species: carcinogen metabolism and biomarkers for carcinogen and pollutant exposure. Environ Health Perspect 90:101–109
Strunjak-Perovic I, Coz-Rakovac R, Topic Popovic N (2003) Micronucleus occurrence in diploid and triploid rainbow trout (Oncorhynchus mykiss Walbaum). Vet Med-Czech 48:215–219
Strunjak-Perovic I, Coz-Rakovac R, Topic Popovic N, Jadan M (2009a) Seasonality of nuclear abnormalities in gilthead sea bream Sparus aurata (L.) erythrocytes. Fish Physiol Biochem 35:287–291
Strunjak-Perovic I, Topic Popovic N, Coz-Rakovac R, Jadan M (2009b) Nuclear abnormalities of marine fish erythrocytes. J Fish Biol 74:2239–2249
Sula E, Aliko V, Pagano M, Faggio C (2019) Digital light microscopy as a tool in toxicological evaluation of fish erythrocyte morphological abnormalities. Microsc Res Tech 83:362–369
Summak S, Aydemir NC, Vatan O, Yılmaz D, Zorlu T, Bilaloglu R (2010) Evaluation of genotoxicity from Nilufer stream (Bursa/Turkey) water using piscine micronucleus test. Food Chem Toxicol 48:2443–2447
Suter GW (2006) Ecological risk assessment. CRC Press, Boca Raton
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 Environ Carcinog Ecotoxicol Rev 29:250–275
Talapatra SN, Banerjee SK (2007) Detection of micronucleus and abnormal nucleus in erythrocytes from the gill and kidney of Labeo bata cultivated in sewage-fed fish farms. Food Chem Toxicol 45:210–215
Teles M, Pacheco M, Santos MA (2007) Endocrine and metabolic responses of Anguilla anguilla L. caged in a freshwater-wetland (Pateira de Fermentelos, Portugal). Sci Total Environ 372:562–570
Tomasello B, Copat C, Pulvirenti V, Ferrito V, Ferrante M, Renis M, Sciacca S, Tigano C (2012) Biochemical and bioaccumulation approaches for investigating marine pollution using Mediterranean rainbow wrasse, Coris julis (Linneaus 1798). Ecotoxicol Environ Saf 86:168–175
Torres-Bugarìn O, Zavala-Aguirre JL, Gòmez-RubioP B-OHR, Zuñiga-Gonzà lez G, Garcìa-Ulloa Gòmez M (2007) Potential fish species as genotoxicity biomarkers at lake “La Alberca”, Michoacà n, Mexico. Hidrobiologica 17:75–81 (in Spanish)
Tsangaris C, Vergolyas M, Fountoulaki E, Goncharuk VV (2011a) Genotoxicity and oxidative stress biomarkers in Carassius gibelio as endpoints for toxicity testing of Ukrainian polluted river waters. Ecotoxicol Environ Saf 74:2240–2244
Tsangaris C, Vergolyas M, Fountoulaki E, Nizheradze K (2011b) Oxidative stress and genotoxicity biomarker responses in grey mullet (Mugil cephalus) from a polluted environment in Saronikos gulf, Greece. Arch Environ Contam Toxicol 61:482–490
Tuvikene A, Huuskonen S, Koponen K, Ritola O, Mauer Ü, Lindström-Seppä P (1999) Oil shale processing as a source of aquatic pollution: monitoring of the biologic effects in caged and feral freshwater fish. Environ Health Perspect 107:745–752
Udroiu I (2006) The micronucleus test in piscine erythrocytes. Aquat Toxicol 79:201–204
Ulupinar M, Okumus I (2002) Detection of mutagenic-carcinogenic pollutants in aquatic systems using cytogenetic methods in fish. Turk J Zool 26:141–148
Valskienė R, Baršienė J, Butrimavičienė L, Pažusienė J, Grygiel W, Stankevičiūtė M, Rybakovas A (2019) Induction of nuclear abnormalities in herring (Clupea harengus membras), flounder (Platichthys flesus), and Atlantic cod (Gadus morhua) collected from the southern part of the Gotland Basin – the Baltic Sea (2010-2017). Environ Sci Pollut Res 26:13366–13380
van der Burg B, van der Linden S, Man H-Y, Winter R, Jonker L, van Vugt-Lussenburg B, Brower A (2013) A panel of quantitative Calux® reporter gene assays for reliable high-throughput toxicity screening of chemicals and complex mixtures. In: Steinberg P (ed) High-throughput screening methods in toxicity testing. Wiley, pp 519–532
van der Linden SC, von Bergh AR, van Vught-Lussenburg BM, Jonker LR, Teunis M, Krul CA, van der Burg B (2014) Development of a panel of high-throughput reporter-gene assays to detect genotoxicity and oxidative stress. Mutat Res 760:23–32
van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149
van der Oost R, Sileno G, Janse T, Nguyen MT, Besselink H, Brouwer A (2017a) SIMONI (smart integrated monitoring) as a novel bioanalytical strategy for water quality assessment: part II-field feasibility survey. Environ Toxicol Chem 36:2400–2416
van der Oost R, Sileno G, Suárez-Muñoz M, Nguyen MT, Besselink H, Brouwer A (2017b) SIMONI (smart integrated monitoring) as a novel bioanalytical strategy for water quality assessment: part I-model design and effect-based trigger values. Environ Toxicol Chem 36:2385–2399
Van Ngan P, Gomes V, Passos MJACR, Ussami KA, Campos DYF, Silva Rocha AJ, Pereira BA (2007) Biomonitoring of the genotoxic potential (micronucleus and erythrocyte nuclear abnormalities assay) of the Admiralty Bay water surrounding the Brazilian Antarctic Research Station “Comandante Ferraz”, King George Island. Polar Biol 30:209–217
Venturoti GP, Boldrini-França J, Gomes AS, Chisté B, Gomes LC (2019a) Geophagus brasiliensis (Teleostei: Cichlidae) as an indicator of toxicity of ornamental stone processing wastes. Comp Biochem Physiol C Toxicol Pharmacol 226:108639
Venturoti GP, Boldrini-França J, Kiffer WP, Francisco AP, Gomes AS, Gomes LC (2019b) Toxic effects of ornamental stone processing waste effluents on Geophagus brasiliensis (Teleostei: Cichlidae). Environ Toxicol Pharmacol 72:103268
Viana LF, Súarez YR, Cardoso CAL, Amaral Crispim B, Grisolia AB, Lima-Junior SE (2017) Mutagenic and genotoxic effects and metal contaminations in fish of the Amambai River, upper Paraná River, Brazil. Environ Sci Pollut Res 24:27104–27112
Viana LF, Súarez YR, Cardoso CAL, Amaral Crispim B, Cavalcante DNC, Grisolia AB, Lima-Junior SE (2018a) The response of neotropical fish species (Brazil) on the water pollution: metal bioaccumulation and genotoxicity. Arch Environ Contam Toxicol 75:476–485
Viana LF, Súarez YR, Cardoso CAL, Solórzano JCJ, Amaral Crispim B, Grisolia AB, Lima-Junior SE (2018b) Erythrocyte nuclear abnormalities in Astyanax lacustris in response to landscape characteristics in two neotropical streams. Arch Environ Contam Toxicol 75:327–334
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 12:153–164
Vieira CED, Costa PG, Lunardelli B, de Oliveira LF, da Costa CL, 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 542:44–56
Viganò L, Camoirano A, Izzotti A, D’Agostini F, Polesello S, Francisci C, De Flora S (2002) Mutagenicity of sediments along the Po River and genotoxicity biomarkers in fish from polluted areas. Mutat Res 515:125–134
Vosyliene MZ, Kazlauskiene N, Baršienė J, Andreikenaite L, Milukaite A, Taujanskis E (2010) Ecotoxicity and genotoxicity relating to fish in wastewaters discharged from the Vilnius treatment plant. Water Sci Technol 62:859–865
Wachtel CC, Oliveira EC, Maniglia TC, Smith-Johannsen A, Almeida Roque A, Castilhos Ghisi N (2019) Waterborn genotoxicity in Southern Brazil using Astyanax bifasciatus (Pisces: Teleostei). Bull Environ Contam Toxicol 102:59–65
Walia GK, Handa D, Kaur H, Kalotra R (2015) Ecotoxicological studies on fish, Labeo rohita exposed to tannery industry effluent by using micronucleus test. Nucleus 58:111–116
Wernersson A-S, Carere M, Maggi C, Tusil P, Soldan P, James A, Sanchez W, Dulio V, Broeg K, Reifferscheid G, Buchinger S, Maas H, Van Der Grinten E, O'Toole S, Ausili A, Manfra L, Marziali L, Polesello S, Lacchetti I, Mancini L, Lilja K, Linderoth M, Lundeberg T, Fjällborg B, Porsbring T, Larsson DGJ, Bengtsson-Palme J, Förlin L, Kienle C, Kunz P, Vermeirssen E, Werner I, Robinson CD, Lyons B, Katsiadaki I, Whalley C, den Haan K, Messiaen M, Clayton H, Lettieri T, Carvalho RN, Gawlik BM, Hollert H, Di Paolo C, Brack W, Kammann U, Kase R (2015) The European technical report on aquatic effect-based monitoring tools under the water framework directive. Environ Sci Eur 27:7
White PA, Rasmussen JB (1998) The genotoxic hazards of domestic wastes in surface waters. Mutat Res 410:223–236
Wirzinger G, Weltje L, Gercken J, Sordyl H (2007) Genotoxic damage in field-collected three-spined sticklebacks (Gasterosteus aculeatus L.): a suitable biomonitoring tool? Mutat Res 628:19–30
Witeska M (2013) Erythrocytes in teleost fishes: a review. Zool Ecol 23:275–281
Würgler FE, Kramers PGN (1992) Environmental effects of genotoxins (eco-genotoxicology). Mutagenesis 7:321–327
Zakhidov ST, Chebotareva YV, Savvaitova KA, Maksimov VA (1996) A cytogenetic study of hemopoietic cells in fish from water bodies of the Norilo-Pyasinsk water system (Taimyr). Biol Bull 23:5–9
Zapata-Restrepo LM, Orozco-JimĂ©nez LY, Rueda-Cardona M, EchavarrĂa SL, Mena-Moreno N, Palacio-Baena JA (2017) EvaluaciĂłn genotĂłxica del agua del RĂo Grande (Antioquia, Colombia) mediante frecuencia de eritrocitos micronucleados de Brycon henni (Characiformes: Characidae). Rev Biol Trop 65:405–414 (in Spanish)
Zhang W, Liu W, Zhang J, Zhao H, Zhang Y, Quan X, Jin Y (2012) Characterisation of acute toxicity, genotoxicity and oxidative stress posed by textile effluent on zebrafish. J Environ Sci 24:2019–2027
Zhang J, Chen S, Zhang Y, Quan X, Zhao H, Zhang Y (2014) Reduction of acute toxicity and genotoxicity of dye effluent using Fenton-coagulation process. J Hazard Mater 274:198–204
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D’Agostini, F., La Maestra, S. (2021). Micronuclei in Fish Erythrocytes as Genotoxic Biomarkers of Water Pollution: An Overview. In: de Voogt, P. (eds) Reviews of Environmental Contamination and Toxicology Volume 258. Reviews of Environmental Contamination and Toxicology, vol 258. Springer, Cham. https://doi.org/10.1007/398_2021_76
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