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In the Upper Valley of Río Negro and Río Neuquén in Argentina, agriculture represents the second most important economic activity. Azinphos-methyl has been found in water from this region throughout the year at a maximum concentration of 22.48μgL-1 during the application period. Toxicological studies on local non-target species have been performed mostly on vertebrates, while mollusks, which could be more sensitive, have not been studied so far. This work aims to characterize cholinesterase (ChE) and carboxilesterase (CE) activities of Chilina gibbosa, a freshwater gastropod native to southern Argentina and Chile. These enzymes, together with neurotoxicity signals, are evaluated herein after as sensitive biomarkers of exposure to azinphos-methyl at environmentally relevant concentrations. Effects of azinphos-methyl on antioxidant defenses: glutathione (GSH), catalase (CAT), superoxide dismutase (SOD) and glutathione S-transferase (GST) are also studied in order to complete a set of biomarkers with different sensitivity and specificity, to propose C. gibbosa as a sentinel species. The highest specific activity was obtained with acetylthiocholine as substrate, followed by propionylthiocholine (83% in comparison to acetylthiocholine) and butyrylthiocholine (19%).The lowest Km and the highest efficiency for ChE were obtained with acetylthiocholine. Regarding CEs activities, a higher efficiency was obtained with p-nitrophenyl butyrate than with p-nitrophenyl acetate. Eserine produced significant inhibition of ChE activity (81% with 0.001mM and 98% with 1mM) while iso-OMPA did not produce any significant effect on ChE. Our results show that C. gibbosa ChE is very sensitive to azinphos-methyl (CI50 0.02μgL-1) while CEs are inhibited at higher concentrations (CI50 1000μgL-1). CEs have been reported to be more sensitive to OPs than ChEs in most of the aquatic invertebrates protecting the organisms from neurotoxic effects. In contrast, C. gibbosa, has ChE which are much more sensitive to azinphos-methyl than CEs and shows marked signs of neurotoxicity. Regarding antioxidant defenses, GSH levels were significantly increased by 0.02 and 20μgL-1 azinphos-methyl (80 and 103%, respectively), CAT activity was increased 85% only at 0.02μgL-1 and SOD and GST did not show any significant response. Since ChE activity, neurotoxicity signs, GSH and CAT are sensitive biomarkers of acute exposure to azinphos-methyl at environmental concentrations C. gibbosa could be included as sentinel species in monitoring programs of pesticide hazard in regions of Argentina and Chile. © 2013 Elsevier B.V.


Documento: Artículo
Título:Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in a freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases
Autor:Bianco, K.; Yusseppone, M.S.; Otero, S.; Luquet, C.; Ríos de Molina, M.D.C.; Kristoff, G.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Nuñez, 1428, Buenos Aires, Argentina
IQUIBICEN-CONICET, Ciudad Universitaria, Nuñez, 1428, Buenos Aires, Argentina
Laboratorio de Ecotoxicología Acuática (INBIOMA CONICET-UNCo), Junín de los Andes, Neuquén, Argentina
Palabras clave:Antioxidant defenses; Azinphos-methyl; B-esterases; Biomarkers; Invertebrates; 4 nitrophenyl acetate; acetylthiocholine; azinphos methyl; butyric acid 4 nitrophenyl ester; butyrylthiocholine; carboxylesterase; catalase; choline derivative; cholinesterase; glutathione; glutathione transferase; nitrogen derivative; organophosphate insecticide; physostigmine; propionylthiocholine; superoxide dismutase; unclassified drug; antioxidant; biomarker; ecotoxicology; enzyme activity; gastropod; insecticide; organophosphate; toxicity; acute toxicity; animal experiment; animal tissue; article; Chilina gibbosa; controlled study; enzyme activity; enzyme substrate; gastropod; IC 50; neurotoxicity; nonhuman; priority journal; sensitivity and specificity; Argentina; Neuquen Basin; Rio Negro [Argentina]; 1-chloro-2,4-dinitrobenzene; 5,5′-dithio-2-bis-nitrobenzoate; 50% inhibition concentration; acetylthiocholine iodide; Antioxidant defenses; ASCh; Azinphos-methyl; B-esterases; Biomarkers; BSCh; butyrylthiocholine iodide; carboxylesterase; CAT; catalase; CDNB; CE; ChE; cholinesterase; DTNB; glutathione; glutathione S-transferase; GSH; GST; IC(50); Invertebrates; iso-OMPA; NOEC; OP; organophosphate insecticide; p-nitrophenyl acetate; p-nitrophenyl butyrate; p-NPA; p-NPB; propionylthiocholine iodide; PrSCh; SOD; superoxide dismutase; tetraisopropyl pyrophosphoramide; the no observed effect concentration; Animals; Argentina; Biological Markers; Carboxylic Ester Hydrolases; Cholinesterases; Environmental Monitoring; Gastropoda; Insecticides; Motor Activity; Nervous System; Organophosphorus Compounds; Water Pollutants, Chemical
Página de inicio:26
Página de fin:35
Título revista:Aquatic Toxicology
Título revista abreviado:Aquat. Toxicol.
CAS:4 nitrophenyl acetate, 830-03-5; acetylthiocholine, 1797-69-9, 4468-05-7; azinphos methyl, 86-50-0; butyric acid 4 nitrophenyl ester, 2635-84-9; butyrylthiocholine, 1866-16-6, 4555-00-4; carboxylesterase, 59536-71-9, 83380-83-0, 9016-18-6, 9028-01-7; catalase, 9001-05-2; cholinesterase, 9001-08-5; glutathione, 70-18-8; glutathione transferase, 50812-37-8; physostigmine, 57-47-6, 64-47-1; propionylthiocholine, 24578-90-3; superoxide dismutase, 37294-21-6, 9016-01-7, 9054-89-1


  • Aldridge, W.N., Two types of esterases (A and B) hydrolysing p-nitrophenyl acetate, propionate and butyrate, and a method for their determination (1953) Biochem. J., 53, pp. 110-117
  • Al-Ghais, S.M., Ahmads, S., Ali, B., Differential inhibition of xenobiotic-metabolizing carboxulesterases by organotins in marine fish (2000) Ecotoxicol. Environ. Saf., 46, pp. 258-264
  • Anguiano, O.L., Ferrari, A., Soleño, J., Martínez, M.C., Venturino, A., Pechen de D Angelo, A.M., Montagna, C.M., Enhanced esterase activity snd resistance to azinphosmethyl in target and nontarget organisms (2008) Environ. Toxicol. Chem., 27, pp. 2117-2123
  • Anguiano, O.L., Catro, C., Venturino, A., Ferrari, A.,, Acute toxicity and biochemical effects of azinphos metthyl in the amphipod Hyalella curvispina.doi:10.1002/tox.21834; Basack, S.B., Oneto, M.L., Fuchs, J.S., Wood, E.J., Kesten, E.M., Esterases of Corbicula fluminea as biomarkers of exposure to organophosphorus pesticides (1998) Bull. Environ. Contam. Toxicol., 61, pp. 569-576
  • Barata, C., Solayan, A., Porte, C., Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna (2004) Aquat. Toxicol., 66, pp. 125-139
  • Barata, C., Damasio, J., López, M.A., Kuster, M., López de Alda, M., Barceló, D., Riva, M.C., Raldúa, D., Combined use of biomarkers and in situ bioassays in Daphnia magna to monitor environmental hazards of pesticides in the Field (2007) Environ. Toxicol. Chem., 26, pp. 370-379
  • Beauchamp, C., Fridovich, I., Superoxide dismutase: improved assays and an assay applicable to acrylamide gels (1971) Anal. Biochem., 44, pp. 276-287
  • Bocquené, G., Roig, A., Fournier, D., Cholinesterases from the common oyster (Crassostrea gigas). Evidence for the presence of a soluble acetylcholinesterase insentive to organophosphate and carbamate inhibitors (1997) FEBS Lett., 407, pp. 261-266
  • Bosnia, A.S., Kaisin, F.J., Tablado, A., Population dynamics and production of the freshwater snail Chilina gibbosa Sowerby 1841 (Chilinidae, Pulmonata) in a North-Patagonian reservoir (1990) Hydrobiología, 190, pp. 97-110
  • Cacciatore, L.C., Kristoff, G., Verrengia Guerrero, N., Cochón, A., Binary mixtures of azinphos-methyl oxon and chlorpyrifos oxon produce in vitro synergistic cholinesterase inhibition in Planorbarius corneus (2012) Chemosphere, 88, pp. 450-458
  • Cacciatore, L.C., Verrengia Guerrero, N.R., Cochón, A., Cholinesterase and carboxylesterase inhibition in Planorbarius corneus exposed to binary mixtures of azinphos-methyl and chlorpyrifos (2013) Aquat. Toxicol., pp. 124-134
  • Cao, C., Leng, Y., Kufe, D., Catalase activity is regulated by c-Abl and Arg in the oxidative stress response (2003) J. Biol. Chem., 278, pp. 29667-29675
  • Claiborne, A., Catalase activity (1985) CRC Handbook of Methods for Oxygen Radical Research, pp. 283-284. , CRC Press, Boca Raton, FL, R. Greenwald (Ed.)
  • Cooper, N.L., Bidwell, J.R., Cholinesterase inhibition and impacts on behavior of the Asian clam, Corbicula fluminea, after exposure to an organophosphate insecticide (2006) Aquat. Toxicol., 76, pp. 258-267
  • Dickinson, D.A., Forman, H.J., Cellular glutathione and thiols metabolism (2002) Biochem. Pharmacol., 64, pp. 1019-1026
  • Di Giulio, R.T., Washburn, P.C., Wenning, R.J., Winston, G.W., Jewell, C.S., Biochemical responses in aquatic animals: a review of determinants of oxidative stress (1989) Environ. Toxicol. Chem., 8, pp. 1103-1123
  • Domingues, I., Guilhermino, L., Soares, A.M.V.M., Nogueira, A.J.A., Assessing dimethoate contamination in temperate and tropical climates: Potencial use of biomarkers in bioassays with two chironomid species (2007) Chemosphere, 69, pp. 145-154
  • Ellman, G.L., Tissue sulfydril groups (1959) Arch. Biochem. Biophys., 82, pp. 70-77
  • Ellman, G.L., Courtney, K.D., Andres, V., Featherstone, R.M., A new and rapid colorimetric determination of acetylcholinesterase activity (1961) Biochem. Pharmacol., 7, pp. 88-95
  • Escartín, E., Porte, C., The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring (1997) Environ. Toxicol. Chem., 16, pp. 2090-2095
  • Ferrari, A., Anguiano, O.L., Soleno, J., Venturino, A., Pechen de D' Angelo, A.M., Different susceptibility of two aquatic vertebrates (Oncorhynchus mykiss and Bufo arenarum) to azinphos methyl and carbaryl (2004) Comp. Biochem. Physiol., 139, pp. 239-243
  • Ferrari, A., Lascano, C., Anguiano, O.L., Pechén de D'Angelo, A.M., Venturino, A., Antioxidant responses to azinphos methyl and carbaryl during the embriogenic development of the toad Rhinella (Bufo) arenarum Hensel (2009) Aquat. Toxicol., 93, pp. 37-44
  • Ferrari, A., Venturino, A., Pechen de D'Angelo, A.M., Time course of brain cholinesterase inhibition and recovery following acute and subacute azinphos methyl, parathion and carbaryl exposure in the goldfish (Carassius auratus) (2004) Ecotoxicol. Environ. Saf., 57, pp. 420-425
  • Ferrari, A., Venturino, A., Pechén de D'Angelo, A.M., Effects of carbaryl and azinphos methyl on juvenile rainbow trout (Oncorhynchus mykiss) detoxifying enzymes (2007) Pestic. Biochem. Phys., 88, pp. 134-142
  • Ferriz, R.A., Algunos aspectos de la dieta de cuatro species ícticas del río Limay (Argentina) (1993) Rev. Ictiología, pp. 1-7
  • Fuentealba, C., Figueroa, R., Monroe, J.J., Endemism analysis of chilean freshwater mollusks (2010) Rev. Chilena Historia Natural, 83, pp. 289-298
  • Gagnaire, B., Geffard, O., Xuereb, B., Margoum, C., Garric, J., Cholinesterase activities as potential biomarkers: Characterzation in two freshwater snails, Potamopyrgus antipodarum (Mollusca, Hydrobiidae, Smith 1889) and Valvata piscinalis (Mollusca, Valvatidae, Muller 1774) (2008) Chemosphere, 71, pp. 553-560
  • González Vejares, S., Sabat, P., Sanchez-Hernandez, J.C., Tissue-specific inhibition and recovery of esterase activities in Lumbriculs terrestres experimentally exposed to chlorpyrifos (2010) Comp. Biochem. Physiol., 151, pp. 351-359
  • Galloway, T.S., Millward, N., Brownw, M.A., Depledge, M.H., Rapid assessment of organophosphorus/carbamate exposure in the bivalve mollusk Mytilus edulis using combined esterase activities as biomarkers (2002) Toxicology, 61, pp. 169-180
  • Granovsky, A.V., Ma, L., Ricaud, R., Bengtson, R.L., Selim, H.M., Fate of azinphosmethyl in a sugarcane field: distributions in canopy, soil, and runoff (1996) J. Environ. Qual., 25, pp. 1210-1216
  • Habig, W.H., Pabst, M.J., Kakoby, W.B., Glutathione S-transferases. The first enzymatic step in mercapturic acid formation (1974) J. Biol. Chem., 249, pp. 7130-7139
  • Jokanovic, M., Biotransformation of organophosphorus compounds (2001) Toxicology, 166, pp. 139-160
  • Kim, J., Kim, S., An, K.W., Choi, C.Y., Lee, S., Choi, K., Molecular cloning of Daphnia magma catalase and its biomarker potential against oxidative stress (2010) Comp. Biochem. Physiol., 152, pp. 263-269
  • Klosterhaus, S.L., Di Pinto, L.M., Chandler, G.T., A comparative assessment of azinphosmethyl bioaccumulation and toxicity in two estuarine meiobenthic harpacticoid copepods (2003) Environ. Toxicol. Chem., 22, pp. 2960-2968
  • Kristoff, G., (2010) Estudio Comparativo de Biomarcadores en los Invertebrados Acuáticos Biomphalaria glabrata y Lumbriculus variegatus Expuestos a Pesticidas de Relevancia Ambiental, , Tesis de Doctorado, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
  • Kristoff, G., Cacciatore, L.C., Verrengia Guerrero, N.R., Cochón, A.C., Effects of the organophosphate insecticide azinphos-methyl on the reproduction and cholinesterase activity of Biomphalaria glabrata (2011) Chemosphere, 84, pp. 585-591
  • Kristoff, G., Chiny Barrionuevo, D., Cacciatore, L.C., Verrengia Guerrero, N.R., Cochón, A., In vivo studies on inhibition and recuperation of B-esterase activity in Biomphalaria glabrata exposed to azinphos-methyl: analysis of enzyme, substrate and tissue dependence (2012) Aquat. Toxicol., pp. 19-26
  • Kristoff, G., Verrengia Guerrero, N., Cochón, A., Effects of azinphos-methyl exposure on enzymatic and non-enzymatic antioxidant defenses in Biomphalaria glabrata and Lumbriculus variegatus (2008) Chemosphere, 72, pp. 1333-1339
  • Kristoff, G., Verrengia Guerrero, N.R., Cochón, A.C., Inhibition of cholinesterases and carboxylesterases of two invertebrate species, Biomphalaria glabrata and Lumbriculus variegatus, by the carbamate pesticide carbaryl (2010) Aquat. Toxicol., 96, pp. 115-123
  • Kristoff, G., Verrengia Guerrero, N.R., Pechén de D'Angelo, A.M., Cochón, A.C., Inhibition of cholinesterase activity by azinphos-methyl in two freshwater invertebrates: Biomphalaria glabrata and Lumbriculus variegatus (2006) Toxicology, 222, pp. 185-194
  • Lascano, C.I., Ferrari, A., Gauna, L.E., Cocca, C., Cochón, A.C., Verrengia Guerrero, N., Venturino, A., Organophosphorus insecticidas affect normal polyamine metabolism in amphibian embryogenesis (2011) Pest. Biochem. Physiol., 101, pp. 240-247
  • Laguerre, C., Sánchez-Hernández, J., Köhler, H.R., Triebskorn, R., Capowiez, Y., Rault, M., Mazzia, C., B-type esterases in the snail Xeropicta derbentina: An enzymological analysis to evaluate their use as biomarkers of pesticide exposure (2009) Environ. Pollut., 157, pp. 199-207
  • Lehtonen, K.K., Leinio, S., Effects of exposure to cooper and malathion on metallothionein levels and acetylcholinesterase activity of the mussel Mytilus edulis and the clam Macoma balthica from the northern Baltic sea (2003) Bull. Environ. Contam. Toxicol., 71, pp. 489-496
  • Leung, K.M.Y., Grist, E.P.M., Morley, N.J., Morritt, D., Crane, M., Chronic toxicity of tributyltin on development and reproduction of the European freshwater snail Lymnaea stagnalis (L.) (2007) Chemosphere, 66, pp. 1358-1366
  • Livingstone, D.R., Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms (2001) Mar. Pollut. Bull., 42, pp. 656-666
  • Loewy, M., Kirs, V., Carvajal, G., Venturino, A., Pechén de D'Angelo, A.M., Groundwater contamination by azinphos methyl in the Northern Patagonic Region (Argentina) (1999) Sci. Total Environ., 225, pp. 211-218
  • Loewy, R.M., Monza, L.B., Kiers, V.E., Savini, M.C., Pesticide distribution in an agricultural environment in <PL>Argentina</PL> (2011) J. Environ. Sci. Health B, 46, pp. 662-670
  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the folin phenol reagent (1951) J. Biol. Chem., 193, pp. 265-275
  • Milatovic, D., Gupta, R.C., Aschner, M., Anticholinesterase toxicity and oxidative stress (2006) Scient. World J., 28, pp. 295-310
  • Mora, P., Fournier, D., Narbonne, J.F., Cholinesterases from the marine mussels Mytilus galloprovincialis L. and M. Edulis L. and from the freshwater bivalve Corbicula fluminea Muller (1999) Comp. Biochem. Physiol., 122 C, pp. 353-361
  • Mora, P., Michel, X., Narbonne, J.F., Cholinesterase activity as potencial biomarker in two bivalves (1999) Environ. Toxicol. Pharmacol., 7, pp. 253-260
  • Biological markers in environmental health research (1987) Environ. Health Perspect., 74, pp. 3-9. , NRC.Committee on Biological Markers of the National Research Council
  • Oliveira-Filho, E.C., Koppe Grisolia, C., Roma Paumgartten, F.J., Transgeneration study of the effects of nonylphenol ethoxylate on the reproduction of the snail Biomphalaria tenagophila (2009) Ecotoxicol. Environ. Saf., 72, pp. 458-465
  • O'Neill, A.J., Galloway, T.S., Browne, M.A., Dissanayake, A., Depledge, M.H., Evaluation of toxicity in tributaries of the Mersey estuary using the isopod Asellus aquaticus (L.) (2004) Mar. Environ. Res., 58, pp. 327-331
  • Oruc, O.E., Sevgiler, Y., Uner, N., Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl (2004) Comp. Biochem. Physiol. Part C, 137, pp. 43-51
  • Peña-Llopis, S., Ferrando, M.D., Peña, J.B., Impaired glutathione redox status is associated with decreased survival in two organophosphate-poisoned marine bivalves (2002) Chemosphere, 47, pp. 485-497
  • Pope, C.N., Organophosphorus pesticides: do they have all the same mechanism of toxicity? (1999) J. Toxicol. Environ. Health., Part B, 2, pp. 161-181
  • Rivadeneira, P.R., Agrelo, M., Otero, S., Kristoff, G., Different effects of subchronic exposure to low concentrations of the organophosphate insecticide chlorpyrifos in a freshwater gastropod (2013) Ecotoxicol. Environ. Saf., 90, pp. 82-88
  • Rumi, A., Gutierrez Gregoric, D.E., Núñez, V., Darrigan, G.A., Malacología Latinoamericana. Moluscos de agua dulce de Argentina (2008) Rev. Biol. Trop., 56, pp. 77-111
  • Sanchez-Hernandez, J.C., Ecotoxicological perspectives of B-esterases in the assessment of pesticide contamination (2007) Environmental Pollution: New Research, pp. 1-45. , Nova Science Publishers, Inc, N.Y., USA, R.H. Plattenberg (Ed.)
  • Sanchez-Hernandez, J.C., Wheelock, C.E., Tissue distribution, isozyme abundance and sensitivity to chorpyrifos-oxon of carboxylesterases in the earthworm Lumbricus terrestris (2009) Environ. Pollut., 157, pp. 264-272
  • Scandalios, Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses (2005) Braz. J. Med. Biol. Res., 38, pp. 995-1014
  • Schulz, R., Field studies on exposure, effects, and risk mitigation of aquatic nonpoint-source insecticide pollution: a review (2004) J. Environ. Qual., 33, pp. 419-448
  • (2005), Secretaría de Recursos Hídricos de la Nación, Valores guías para la protección de la vida acuática en agua dulce; Strange, R.C., Jones, P.W., Fryer, A.A., Glutathione S-transferase: genetics and role in toxicology (2000) Toxicol. Lett., pp. 357-363
  • Strong, E.E., Garcominy, O., Ponder, W.F., Bouchet, P., Global diversity of gastropods (Gastropoda; Mollusca) in freshwater (2008) Hydrobiolgía, 595, pp. 149-166
  • Talesa, V., Contenti, S., Mangiabene, C., Pascolini, R., Rosi, G., Principato, G.B., Propionylcholinesterase from Murex brandaris: comparison with other invertebrate cholinesterases (1990) Comp. Biochem. Physiol., 96 C, pp. 39-43
  • Tossi, A.P., Pechen de D'Angelo, A.M., Savini, M.C., Loewy, R.M., Assessing pesticide hazards on surface water from the northern patagonian región Argentina (2009) Acta Toxicol. Argent., 17, pp. 1-7
  • Tripathi, P.K., Singh, A., Carbaryl induced alterations in the reproduction and metabolism of the freshwater snail Lymnaea acuminata (2004) Pest. Biochem. Physiol., 79, pp. 1-9
  • (2001), US EPA, United States Environmental Protection Agency, Interim registration eligibility decision for azinphos-methyl. Case No. 0235; Valdovinos, C., Estado de conocimiento de los gasterópodos dulceacuícolas de Chile (2006) Gayana, 70, pp. 88-95
  • van der Oost, R., Beyer, J., Vermeulen, N.P.E., Fish bioaccumulation and biomarkers in environmental risk assessment: a review (2003) Environ. Toxicol. Pharmacol., 13, pp. 57-149
  • Varó, I., Navarro, J.C., Amat, F., Guilhermino, L., Characterization of cholinesterases and evaluation of the inhibitory potential of chlorpyrifos and dichlorvos to Artemia salina and Artemia parthenogenetica (2002) Chemosphere, 48, pp. 563-569
  • Venkateswara Rao, J., Sublethal effects of an organophosphorus insecticide (RPR-11) on biochemical parameters of tilapia, Oreochromis mossambicus (2006) Comp. Biochem. Physiol., 143 C, pp. 492-498
  • Venturino, A., Anguiano, O.L., Gauna, L., Cocca, C., Bergoc, R.M., Pechén de D'Angelo, A.M., Thiols and polyamines in the potentiation of malathion toxicity in larval stages of the toad Bufo arenarum (2001) Comp. Biochem. Physiol., 130 C, pp. 191-198
  • Verma, R.S., Mehta, A., Srivastava, N., In vivo clorpyrifos induced oxidative stress: attenuation by antioxidant vitamins (2007) Pestic. Biochem. Physiol., 88, pp. 191-196
  • Wan, M.T., Szeto, S.Y., Price, P., Distribution and persistence of azinphos-methyl and parathion in chemigated cranberry bogs (1995) J. Environ. Qual., 24, pp. 589-596
  • Wheelock, C.E., Phillips, B.M., Anderson, B.S., Miller, M.J., Hammock, B.D., Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs) (2008) Rev. Environ. Contam. Toxicol., 195, pp. 117-178
  • Wheelock, C.E., Shan, G., Ottea, J., Overview of carboxylesterases and their role in the metabolism of insecticides (2005) J. Pest. Sci., 30, pp. 75-83
  • Whitehead, A., Anderson, S.L., Ramirez, A., Wilson, B.W., Cholinesterases in aquatic biomonitoring: assay optimization and species-specific characterization for a California native fish (2005) Ecotoxicology, 14, pp. 597-606
  • Wogram, J., Sturm, A., Segner, H., Liess, M., Effects of parathion on acetylcholinesterase, butyrylcholinesterase, and carboxylesterase in three-spined stickleback (Gasterosteus aculeatus) following short-term exposure (2001) Environ. Toxicol. Chem., 20, pp. 1528-1531
  • Xuereb, B., Noury, P., Felten, V., Garric, J., Geffard, O., Cholinesterase activity in Gammarus pulex (Crustacea Amphipoda): Characterization and effects of chlorpyrifos (2007) Toxicology, 236, pp. 178-189


---------- APA ----------
Bianco, K., Yusseppone, M.S., Otero, S., Luquet, C., Ríos de Molina, M.D.C. & Kristoff, G. (2013) . Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in a freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases. Aquatic Toxicology, 144-145, 26-35.
---------- CHICAGO ----------
Bianco, K., Yusseppone, M.S., Otero, S., Luquet, C., Ríos de Molina, M.D.C., Kristoff, G. "Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in a freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases" . Aquatic Toxicology 144-145 (2013) : 26-35.
---------- MLA ----------
Bianco, K., Yusseppone, M.S., Otero, S., Luquet, C., Ríos de Molina, M.D.C., Kristoff, G. "Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in a freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases" . Aquatic Toxicology, vol. 144-145, 2013, pp. 26-35.
---------- VANCOUVER ----------
Bianco, K., Yusseppone, M.S., Otero, S., Luquet, C., Ríos de Molina, M.D.C., Kristoff, G. Cholinesterases and neurotoxicity as highly sensitive biomarkers for an organophosphate insecticide in a freshwater gastropod (Chilina gibbosa) with low sensitivity carboxylesterases. Aquat. Toxicol. 2013;144-145:26-35.