Multimarker approach analysis in common carp Cyprinus carpio sampled from three freshwater sites

Environmental Monitoring and Assessment

Volumn 168, Issue 1-4, 2010, Pages 285-298

  Tlili, Sofiene ^a   Jebali, Jamel ^a   Banni, Mohamed ^a   Haouas, Zohra ^b   Mlayah, Ammar ^c   Helal, Ahmed Noureddine ^d   Boussetta, Hamadi ^a  

^a Ecole Superieure d'Horticulture et d'Elevage de Chott Mariem   (Tunisia)

^b UNIVERSITY OF MONASTIR   (Tunisia)

^c University of Carthage   (Tunisia)

^d UNIVERSITY OF MONASTIR   (Tunisia)

Author keywords

Cholinesterases; Cyprinus carpio; Dam lakes; Discriminant analysis; Metallothionein; Multimarker approach

Indexed keywords

CHOLINESTERASE ACTIVITY; CHOLINESTERASES; COMMON CARP; CYPRINUS CARPIO; ECOLOGICAL CHARACTERISTICS; GENOTOXICITIES; GLUTATHIONE-S-TRANSFERASE; METALLOTHIONEINS; MICRONUCLEUS FREQUENCIES; NEUROTOXICITY; PHASE II DETOXIFICATION ENZYME; STRESS INDICATORS;

BRAIN; DAMS; DETOXIFICATION; DISCRIMINANT ANALYSIS; FISH; LAKES;

BIOMARKERS;

BIOLOGICAL MARKER; CHOLINESTERASE; GLUTATHIONE TRANSFERASE; METALLOTHIONEIN; FRESH WATER; MUTAGENIC AGENT; WATER POLLUTANT;

BIOINDICATOR; BIOMARKER; BLOOD; BRAIN; CYPRINID; DETOXIFICATION; ENZYME ACTIVITY; FRESHWATER ENVIRONMENT; GENOTOXICITY; INHIBITION; MUSCLE; SAMPLING;

ANIMAL TISSUE; ARTICLE; BRAIN; CARP; CHEMICAL ANALYSIS; CONTROLLED STUDY; DISCRIMINANT ANALYSIS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; FRESHWATER ENVIRONMENT; GENOTOXICITY; LIVER; MICRONUCLEUS TEST; MUSCLE; NEUROTOXICITY; NONHUMAN; PROTEIN CONTENT; TUNISIA; WATER ANALYSIS; WATER POLLUTION; ANIMAL; CHEMISTRY; DRUG DETOXIFICATION; ENZYMOLOGY; METABOLISM; PROCEDURES; TOXICITY; WATER POLLUTANT;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; CARPS; CHOLINESTERASES; ENVIRONMENTAL MONITORING; FRESH WATER; GLUTATHIONE TRANSFERASE; LIVER; METABOLIC DETOXICATION, PHASE II; METALLOTHIONEIN; MICRONUCLEUS TESTS; MUSCLES; MUTAGENS; TUNISIA; WATER POLLUTANTS, CHEMICAL;

TUNISIA;

CYPRINIDAE; CYPRINUS CARPIO;

EID: 77955418508     PISSN: 01676369     EISSN: 15732959     Source Type: Journal    
DOI: 10.1007/s10661-009-1112-5     Document Type: Article

References (80)

1. K Al-Sabti 2000 Chlorotriazine reactive azo red 120 textile dye induces micronuclei in fish Ecotoxicology and Environmental Safety 47 149 155 10.1006/eesa.2000.1931 1:CAS:528:DC%2BD3cXntFSjt7o%3D
2. K Al-Sabti CD Metcalfe 1995 Fish micronuclei for assessing genotoxicity in water Mutation Research 343 121 135 10.1016/0165-1218(95)90078-0 1:CAS:528:DyaK2MXlvFKks7g%3D
3. ANPE (Agence Nationale de Protection de l'Environnement, Tunisie) (2006). Rapport national de l'état de l'environnement, 262 pp. Tunisian Environment Ministry: Tunis.
4. V Arkhipchuk N Garanko 2002 A novel nucleolar biomarker in plant and animal cells for assessment of substance cytotoxicity Environment Toxicology 17 187 194 10.1002/tox.10056 1:CAS:528:DC%2BD38Xlt1KktLs%3D (Pubitemid 34784963)
5. V Arkhipchuk N Garanko 2005 Using the nucleolar biomarker and the micronucleus test on in vivo fish fin cells Ecotoxicology and Environmental Safety 62 42 52 10.1016/j.ecoenv.2005.01.001 1:CAS:528:DC%2BD2MXlsFCktLk%3D (Pubitemid 40838632)
6. V Arkhipchuk C Blaise M Malinovskaya 2006 Use of hydra for chronic toxicity assessment of waters intended for human consumption Environmental Pollution 142 200 211 10.1016/j.envpol.2005.10.012 1:CAS:528: DC%2BD28Xjs1aisb4%3D
7. T Balint T Szegletes H Szegletes 1995 Biochemical and subcellular changes in carp exposed to the organophosphorus methidathion and pyrethroid deltamethrin Aquatic Toxicology 33 279 295 10.1016/0166-445X(95)00029-4 1:CAS:528:DyaK2MXoslGgtbg%3D
8. M Banni J Jebali M Daubeze C Clerandau H Guerbej JF Narbonne, et al. 2006 Monitoring pollution in Tunisian coasts: Application of a classification scale based on biochemical markers Biomarkers 10 2-3 105 116
9. M Banni F Dondero J Jebali H Guerbej H Boussetta A Viarengo 2007 Assessment of heavy metal contamination using real time PCR analysis of mussel metallothionein mt10 and mt20 expression: A validation along the Tunisian coasts Biomarkers 12 4 369 383 10.1080/13547500701217061 1:CAS:528: DC%2BD2sXmtlGrtrc%3D (Pubitemid 46952299)
10. SM Bello DG Franks JJ Stegeman ME Hahn 2001 Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: In vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes Toxicological Sciences 60 77 91 10.1093/toxsci/60.1.77 1:CAS:528:DC%2BD3MXhslGktrk%3D (Pubitemid 32229829)
11. MM Bradford 1976 A rapid and sensitive method for the quantification of microgram of protein utilizing the principal of protein-dye binding Analytical Biochemistry 72 248 254 10.1016/0003-2697(76)90527-3 1:CAS:528: DyaE28XksVehtrY%3D
12. I Bremner 1987 Interactions between metallothionein and trace elements Program Food Nutrition Sciences 11 1 37 1:CAS:528:DyaL2sXkvFGlurk%3D
13. MP Cajaraville MJ Bebianno J Blasco C Porte C Sarasquete A Viarengo 2000 The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: A practical approach Science of the Total Environment 247 2-3 295 311 10.1016/S0048-9697(99)00499-4 1:CAS:528:DC%2BD3cXhvVKgsrY%3D (Pubitemid 30145681)
14. T Cavas S Ergene-Gozukara 2003 Evaluation of the genotoxic potential of lambdacyhalothrin using nuclear and nucleolar biomarkers on fish cells Mutation Research 534 93 99 1:CAS:528:DC%2BD38Xpslaks7Y%3D
15. T Cavas N Garanko V Arkhipchuk 2005 Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate Food and Chemical Toxicology 43 569 574 10.1016/j.fct.2004.12.014 1:CAS:528:DC%2BD2MXhtlOlsro%3D (Pubitemid 40255292)
16. JE Chambers JS Boone HW Chambers DL Straus 2002 Biomarkers as predictors in health and ecological risk assessment Human and Ecological Risk Assessment 8 1 165 176 10.1080/20028091056809 (Pubitemid 41445958)
17. GM Chuiko 2000 Comparative study of acetylcholinesterase and butyrylcholinesterase in brain and serum of several freshwater fish: Specific activities and in vitro inhibition by DDVP, an organophosphorus pesticide Comparative Biochemistry and Physiology Part C 127 233 242 1:STN:280: DC%2BD3MzgtVelsg%3D%3D
18. Council Directive 98/83/EC (1998). Levels for the quality of water intended for human consumption. www.emwis.org/IFP/law-EU.htm.
19. M Crane W Sildanchandra R Kheir A Callaghan 2002 Relationship between biomarker activity and developmental endpoints in Chironomus riparius Meigen exposed to an organophosphate insecticide Ecotoxicology and Environmental Safety 53 361 369 10.1016/S0147-6513(02)00038-6 1:CAS:528:DC%2BD38XpsFyisbg%3D (Pubitemid 36015989)
20. KE Day IM Scott 1990 Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides Aquatic Toxicology 18 101 114 10.1016/0166-445X(90) 90021-G 1:CAS:528:DyaK3MXjslCmuw%3D%3D (Pubitemid 20373943)
21. G De Boeck TT Huong Ngo K Van Campenhout R Blust 2003 Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure Aquatic Toxicology 65 413 424
22. FR De la Torre L Ferrari A Salibian 2002 Freshwater pollution biomarker: Response of brain acetylcholinesterase activity in two fish species Comparative Biochemistry and Physiology Part C 131 271 280 10.1016/S1096-4959(02)00022-2 (Pubitemid 34214852)
23. FR De la Torre L Ferrari A Salibian 2005 Biomarkers of a native fish species (Cnesterodon decemmaculatus) application to the water toxicity assessment of a peri-urban polluted river of Argentina Chemosphere 59 577 583 10.1016/j.chemosphere.2004.12.039 (Pubitemid 40387790)
24. H De Smet B De Wachter R Lobinski R Blust 2001 Dynamics of (Cd, Zn)-metallothioneins in gills, liver and kidney of common carp Cyprinus carpio during cadmium exposure Aquatic Toxicology 52 269 281 10.1016/S0166-445X(00) 00136-3 (Pubitemid 32175641)
25. DGPA (Direction Générale de Pêche et d'Aquaculture, Tunisie) (2007). Rapport annuel de la pêche continentale dans les barrages tunisiens. Direction Générale de Pêche et Aquaculture (25 pp.). Tunisie: Ministère d'Agriculture et des Ressources Hydrauliques.
26. GL Ellman D Courtneyk V Andres RM Featherstone 1961 A new and rapid colorimetric determination of acetylcholinesterase activity Biochemical Pharmacology 7 88 95 10.1016/0006-2952(61)90145-9 1:CAS:528:DyaF3MXht1Gns7o%3D
27. HI Falfushynska OB Stolyar 2009 Responses of biochemical markers in carp Cyprinus carpio from two field sites in western Ukraine Ecotoxicology and Environmental Safety 72 729 736 10.1016/j.ecoenv.2008.04.006 10.1016/j.ecoenv.2008.04.006 1:CAS:528:DC%2BD1MXhs1Chs7w%3D
28. D Fernandes J Potrykus C Morsiani D Raldùa R Lavado C Porte 2002 The combined use of chemical and biochemical markers to assess water quality in two low-stream rivers (NE Spain) Environmental Research 90 169 178 10.1006/enrs.2002.4390 1:CAS:528:DC%2BD38XovF2nsLY%3D (Pubitemid 35191499)
29. PJ Fitzpatrick J O'Halloran D Sheehan AR Walsh 1997 Assessment of a glutathione-S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L Biomarkers 2 51 56 10.1080/135475097231977 1:CAS:528:DyaK2sXhtV2js7c%3D
30. MH Fulton PB Key 2001 Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects Environmental Toxicology Chemistry 20 37 45 10.1002/etc.5620200104 1:CAS:528:DC%2BD3MXitlOm
31. George, S. G. (1994). Enzymology and molecular biology of phase II xenobiotic-conjugating enzymes in fish. In D. C. Malins, & G. K. Ostrander (Eds.), Aquatic toxicology; molecular, biochemical and cellular perspectives (pp. 37-85). Boca Raton: Lewis.
32. CK Grisolia LRM Starling Fernando 2000 Micronuclei monitoring of fishes from Lake Paranoá, under influence of sewage treatment plant discharges Mutation Research 491 39 44
33. L Guilhermino MN Lacerda AJA Nogueira AMVM Soares 2000 In vitro and in vivo inhibition of Daphnia magna acetylcholinesterase by surfactant agents: Possible implications for contamination biomonitoring Science of the Total Environment 247 137 141 10.1016/S0048-9697(99)00485-4 1:CAS:528: DC%2BD3cXhvVKhu70%3D (Pubitemid 30145666)
34. WH Habig MJ Pabst WB Jakoby 1974 The first enzymatic step in mercapturic acid formation Journal of Biological Chemistry 249 22 7130 7139 1:CAS:528:DyaE2MXltlahtg%3D%3D
35. BH Hansen S Romma OA Garmo PA Olsvik RA Andersen 2006 Antioxidative stress proteins and their gene expression in brown trout (Salmo trutta) from three rivers with different heavy metal levels Comparative Biochemistry and Physiology Part C 143 263 274 1:STN:280:DC%2BD28zlsFSgtQ%3D%3D
36. BH Hansen S Romma LI Softeland PA Olsvik RA Andersen 2006 Induction and activity of oxidative stress-related proteins during waterborne Cu-exposure in brown trout (Salmo trutta) Chemosphere 65 1707 1714 10.1016/j.chemosphere.2006. 04.088 1:CAS:528:DC%2BD28XhtFSrt7rN (Pubitemid 44574421)
37. M Hayashi T Ueada K Uyeno K Wada N Kinae K Saotome, et al. 1998 Development of genotoxicity assays systems that use aquatic organisms Mutation Research 399 125 133 1:CAS:528:DyaK1cXjsVensLk%3D
38. P Hoareau M Gnassia-Barelli M Roméo JP Girard 2001 Differential induction of GST in the clam Ruditapes decussatus European Journal of Biochemistry 269 4359 4366 10.1046/j.1432-1033.2002.03141.x
39. J Jebali M Banni EA Almeida A Bannaoui H Boussetta 2006 Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli Fish Physiology and Biochemistry 32 93 98 10.1007/s10695-006-0041-2 1:CAS:528:DC%2BD28XosFWrsL0%3D (Pubitemid 44288498)
40. J Jebali M Banni H Guerbej H Boussetta J Lopez-Barea J Alhama 2008 Metallothionein induction by Cu, Cd and Hg in Dicentrarchus labrax liver: Assessment by RP-HPLC with fluorescence detection and spectrophotometry Marine Environmental Research 65 358 363 10.1016/j.marenvres.2008.01.002 1:CAS:528:DC%2BD1cXjtVWms7k%3D
41. LY Kim CK Hyun 2006 Comparative evaluation of the alkaline comet assay with the micronucleus test for genotoxicity monitoring using aquatic organisms Ecotoxicology and Environmental Safety 64 288 297 10.1016/j.ecoenv.2005.05.019 1:CAS:528:DC%2BD28XlsVejt74%3D (Pubitemid 43817177)
42. P Kling LJ Erkell P Kille PE Olsson 1996 Metallothionein induction in rainbow Trout Gonadal (RTG-2) cells during free radical exposure Marine Environmental Research 42 33 36 10.1016/0141-1136(95)00081-X 1:CAS:528:DyaK28XjvF2ms7g%3D (Pubitemid 26188750)
43. VI Kozlovskaya FL Mayer OV Menzikova GM Chuyko 1993 Cholinesterase of aquatic animals Reviews of Environmental Contamination & Toxicology 132 117 142 1:CAS:528:DyaK3sXltFelurg%3D
44. R Lavado R Uren R Martin-Skilton A Torreblanca J Del Ramo D Raldu, et al. 2006 The combined use of chemical and biochemical markers to assess water quality along the Ebro River Environmental Pollution 139 330 339 10.1016/j.envpol.2005.05.003 1:CAS:528:DC%2BD2MXht12qu77J (Pubitemid 41770969)
45. AG Leticia GB Gerardo 2008 Determination of esterase activity and characterization of cholinesterases in the reef fish Haemulon plumieris Ecotoxicology and Environmental Safety 71 787 797 10.1016/j.ecoenv.2008.01.024 1:CAS:528:DC%2BD1cXht1Sit77E
46. PA Lopes T Pinheiro MC Santos ML Mathias MJ Collares-Pereira AM Viegas-Crespo 2001 Response of antioxidant enzyme in freshwater fish populations (Leuciscus alburnoides complex) to inorganic pollutants exposure Science of the Total Environment 280 153 163 10.1016/S0048-9697(01)00822-1 1:CAS:528:DC%2BD3MXotFSjsrs%3D (Pubitemid 33009465)
47. S Minissi E Ciccotti M Rizzoni 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 Mutation Research 367 245 251 10.1016/S0165-1218(96)90084-1 1:CAS:528:DyaK28XisFWrtbg%3D (Pubitemid 26125890)
48. JM Monserrat PE Martinez LA Geracitano LL Amado CMG Martins GLL Pinho, et al. 2007 Pollution biomarkers in estuarine animals: Critical review and new perspectives Comparative Biochemistry and Physiology Part C 146 221 234
49. M Monteiro C Quintaneiro F Morgadoa A Soaresa L Guilhermino 2005 Characterization of the cholinesterases present in head tissues of the estuarine fish Pomatoschistus microps: Application to biomonitoring Ecotoxicology and Environmental Safety 62 341 347 10.1016/j.ecoenv.2004.12.007 1:CAS:528:DC%2BD2MXhtFWntrnE (Pubitemid 41430382)
50. C Morales-Caselles ML Martín-Díaz I Riba C Sarasquete TÁ Del Valls 2008 Sublethal responses in caged organisms exposed to sediments affected by oil spills Chemosphere 72 819 825 10.1016/j.chemosphere. 2008.02.060 10.1016/j.chemosphere.2008.02.060 1:CAS:528:DC%2BD1cXmsFylsbo%3D
51. E Ozcan-Oruc D Usta 2007 Evaluation of oxidative stress responses and neurotoxicity potential of diazinon in different tissues of Cyprinus carpio Environmental Toxicology and Pharmacology 23 48 55 10.1016/j.etap.2006.06.005 (Pubitemid 44854648)
52. M Ozmen Z Ayas A Gungurdu GF Ekmekci S Yerli 2007 Ecotoxicological assessment of water pollution in Sariyar Dam Lake, Turkey Ecotoxicology and Environmental Safety 70 163 173 10.1016/j.ecoenv.2007.05.011
53. S Paris-Palacios S Biagianti-Risbourg G Vernet 2003 Metallothionein induction related to hepatic structural perturbations and antioxidative defenses in roach (Rutilus rutilus) exposed to the fungicide procymidone Biomarkers 8 128 141 10.1080/1354750021000050511 1:CAS:528:DC%2BD3sXlt1Crurs%3D (Pubitemid 36747949)
54. A Pathirante SG George 1998 Oxicity of malathion to Nile tilapia, Oreochromis niloticus and modulation by other environmental contaminants Aquatic Toxicology 43 261 271 10.1016/S0166-445X(98)00059-9 (Pubitemid 28556912)
55. JR Pedrajas J Peinado J Lopez-Barea 1995 Oxidative stress in fish exposed to model xenobiotics. Oxidatively modified forms of Cu, Zn superoxide dismutase as potential biomarker Chemico-biological Interactions 98 267 282 10.1016/0009-2797(95)03651-2 1:CAS:528:DyaK2MXps1WktbY%3D (Pubitemid 26027069)
56. N Reddy K Panda V Subhadra B Panda 1995 The allium micronucleus (MNC) assay may be used to distinguish clastogens from aneugens Biologisches Zentralblatt 114 358 368 1:CAS:528:DyaK28Xit1eqt7c%3D
57. H Reynders L Bervoets M Gelders WM De Coen R Blust 2008 Accumulation and effects of metals in caged carp and resident roach along a metal pollution gradient Science of the Total Environment 391 182 195 10.1016/j.scitotenv.2007. 10.056 (Pubitemid 350297351)
58. Rodier, J. (1996). Analyse de l'eau: Eau naturelle, eau résiduaire et eau de mer, 8 Edn. (1381 pp.). Paris: Dunold.
59. G Rodriguez-Fuentes G Gold-Bouchot 2004 Characterization of cholinesterase activity from different tissues of Nile tilapia (Oreochromis niloticus) Marine Environmental Research 58 505 509 10.1016/j.marenvres.2004.03. 037 1:CAS:528:DC%2BD2cXkslSitb4%3D (Pubitemid 38738922)
60. G Roesijadi R Bogumil M Vašák JH Kägi 1998 Modulation of DNA binding of a tramtrack zinc finger peptide by the metallothionein- thionein conjugate pair Journal of Biological Chemistry 273 17425 17432 10.1074/jbc.273.28.17425 1:CAS:528:DyaK1cXkvFaku7o%3D (Pubitemid 28355071)
61. M Roméo RP Cosson M Gnassia-Barelli C Risso X Stien M Lafaurie 1997 Metallothionein determination in the liver of the sea bass Dicentrarchus labrax treated with copper and B(a)P Marine Environmental Research 44 275 284 10.1016/S0141-1136(97)00007-X (Pubitemid 27364128)
62. M Roméo Y Mourgaud A Geffard M Gnassia-Barelli JC Amiard H Budzinski 2003 Multimarker approach in transplanted mussels for evaluating water quality in Charentes, France, coast areas exposed to different anthropogenic conditions Environmental Toxicology 18 295 305 10.1002/tox.10128 (Pubitemid 37258741)
63. A Sturm HC Da Silva De Assis PD Hansen 1999 Cholinesterases of marine teleost fish: Enzymological characterization and potential use in the monitoring of neurotoxic contamination Marine Environmental Research 47 389 398 10.1016/S0141-1136(98)00127-5 1:CAS:528:DyaK1MXhvVyksLc%3D (Pubitemid 29090218)
64. M Tom N Chen M Segev B Herut B Rinkevich 2004 Quantifying fish metallothionein transcript by real time PCR for its utilization as an environmental biomarker Marine Pollution Bulletin 48 705 710 10.1016/j.marpolbul.2003.10.013 1:CAS:528:DC%2BD2cXisVejsL4%3D (Pubitemid 38376247)
65. C Torres de Lemos P Milan Rodel N Regina Terra NC D'Avila de Oliveira B Erdtmann 2007 River water genotoxicity evaluation using micronucleus assay in fish erythrocytes Ecotoxicology and Environmental Safety 66 391 401 10.1016/j.ecoenv.2006.01.004 1:CAS:528:DC%2BD2sXhs1Skt7g%3D (Pubitemid 46204885)
66. I Udroiu 2006 The micronucleus test in piscine erythrocytes Aquatic Toxicology 79 201 204 10.1016/j.aquatox.2006.06.013 1:CAS:528: DC%2BD28Xns1Sksro%3D (Pubitemid 44118455)
67. K Van Campenhout L Bervoets R Blust 2003 Metallothionein concentrations in natural populations of gudgeon (Gobio gobio): Relationship with metal concentrations in tissues and environment Environmental Toxicology and Chemistry 22 1548 1555
68. R Van der Oost P Vindimian J Van Den Brink K Satumalay H Heida NP Vermeulen 1997 Biomonitoring aquatic pollution with feral eel (Anguilla anguilla). Statistical analysis of relationships between contaminant exposure and biomarkers Aquatic Toxicology 39 45 75 10.1016/S0166-445X(96)00851-X (Pubitemid 27264799)
69. R Van der Oost SCC Lopes H Komen K Satumalay 1998 Assessment of environmental quality and inland water pollution using biomarker responses in caged carp (Cyprinus carpio): Use of a bioactivation: Detoxication ratio as a Biotransformation Index (BTI) Marine Environmental Research 46 1-5 315 319
70. R Van Der Oost J Beyer N Vermeulen 2002 Fish bioaccumulation and biomarkers in environmental risk assessment: a review Environmental Toxicology and Pharmacology 13 57 149
71. U Varanasi JE Stein M Nishimento WL Reichert TK Collier 1987 Chemical carcinogenesis in feral fish: Uptake, activation, and detoxification of organic xenobiotics Environmental Health Perspectives 71 155 170 10.2307/3430423 1:CAS:528:DyaL1cXhvVWmsbs%3D
72. A Viarengo 1989 Heavy metals in marine invertebrates, mechanisms of regulation and toxicity at cell level CRC Critical Review in Aquatic Science 1 295 317 1:CAS:528:DyaL1MXkvFWksb0%3D
73. A Viarengo JA Nott 1993 Mechanisms of heavy metals homeostasis in marine invertebrates Comparative Biochemistry and Physiology Part C 104 355 372 10.1016/0742-8413(93)90001-2 (Pubitemid 23167306)
74. A Viarengo E Ponzano F Dondero R Fabbri 1997 A simple spectrophotometric method for metallothionein evaluation in marine organisms: An application to Mediterranean and Antarctic molluscs Marine Environmental Research 44 69 84 10.1016/S0141-1136(96)00103-1 1:CAS:528:DyaK2sXisVKqtrY%3D (Pubitemid 27129456)
75. A Viarengo B Burlando M Cavaletto B Marchi E Ponsano J Blasco 1999 Role of metallothionein against oxidative stress in the mussel Mytillus galloprovincialis American Physiological Society 363 1614 1617
76. A Viarengo D Lowe C Bolognesi E Fabbri A Koehler 2007 The use of biomarkers in biomonitoring: A 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms Comparative Biochemistry and Physiology Part C 146 281 300 1:STN:280:DC%2BD2svls1Onuw%3D%3D
77. L Vigano S Galassi A Arillo 1994 Bioconcentration of polychlorinated biphenyls (PCBs) in rainbow trout caged in the river Po Ecotoxicology and Environmental Safety 28 287 297 10.1006/eesa.1994.1053 1:CAS:528: DyaK2cXls1entbY%3D (Pubitemid 24250829)
78. L Vigano A Arillo F Melodia M Bagnasco C Bennicelli S De Flora 1995 Hepatic and biliary biomarkers in rainbow trout injected with sediment extracts from the river Po (Italy) Chemosphere 30 2117 2128 10.1016/0045-6535(95)00092-M 1:CAS:528:DyaK2MXmt1Whsbo%3D
79. L Vigano A Camoirano A Izzotti F D'Agostini S Polesello C Francisci, et al. 2002 Mutagenicity of sediments along the Po River and genotoxicity biomarkers in fish from polluted areas Mutation Research 515 125 134 1:CAS:528:DC%2BD38XitFWku74%3D
80. Walker, C. H., & Thompson, H. M. (1991). Phylogenetic distribution of cholinesterases and related esterases. In P. Mineau (Ed.), Cholinesterase- inhibiting insecticides. Their impact on wildlife and the environment (pp. 3-19). Amsterdam: Elsevier.