Liver damages and nuclear abnormalities in erythrocytes of Atherinella brasiliensis (Actynopterigii, Atherinopsidade) from two beaches in Southeast of Brazil

Fernandez, Welingtom S.; Dias, June Ferraz; Ribeiro, Ciro Alberto Oliveira; Azevedo, Juliana de Souza

Abstracts

There are few environmental studies using biomarkers for the species Atherinella brasiliensis in Brazil. In the present work, the presence of hepatic histopathological lesions and nuclear abnormalities in erythrocytes were investigated in A. brasiliensis from Lamberto, a beach under influence of domestic wastes and marine activities. For comparison, fish were also sampled in Puruba, a non-polluted beach, located in the northeastern of São Paulo State. The frequency of lesions found in liver was in higher numbers in individuals from Lamberto than Puruba beach. The most critical injuries observed in A. brasiliensis were the presence of necrotic areas, leucocytes infiltration and piknotic nucleus. A high occurrence of cells with vacuolization was also observed. The hepatic lesion index of the fish from Lamberto beach showed significant high values (Iorg=13) when compared with fish from Puruba beach (Iorg=7) suggesting the influence of the several human activities in the studied site. Notched and blebed nucleous were observed in this study, and significant differences were found between the studied sites. However, these differences did not reflect the total nuclear alterations.

histopathology; nuclear abnormalities; Atherinella brasiliensis; biomonitoring; Brazilian Coast

Existem poucos estudos no Brasil usando biomarcadores em Atherinella brasiliensis. No presente trabalho foram investigadas a presença de lesões histopatológicas hepáticas e as alterações nucleares em eritrócitos de A. brasiliensis amostrados na praia do Lamberto, local submetido à influência de resíduos domésticos e atividades humanas. Para comparação, indivíduos da espécie foram também amostrados na praia de Puruba, local não impactado, localizado no noroeste do estado de São Paulo. Peixes provenientes da praia do Lamberto apresentaram lesões hepáticas em número maior do que aqueles da praia de Puruba. Áreas necróticas, infiltração de leucócitos e núcleos picnóticos foram os danos de maior importância observados em A. brasiliensis, apesar de uma elevada ocorrência de vacuolização também ter sido verificada. O índice de lesão hepática dos peixes da praia do Lamberto mostrou valores significantemente maiores (Iorg=13) quando comparados com o dos peixes da praia de Puruba (Iorg=7), sugerindo influência das diversas atividades humanas existentes na área avaliada. Em relação aos núcleos "notched" e "blebed", foram observadas diferenças significativas entre as áreas, mas não para as alterações nucleares totais.

histopatologia; alterações nucleares; Atherinella brasiliensis; biomonitoramento; costa brasileira

AKAISHI, F. M.; ST-JEAN, S. D.; BISHAY, F.; CLARKE, J.; RABITTO, I. S.; OLIVEIRA RIBEIRO, C.A. Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquat. Toxicol., v. 82, n. 1, p. 1-14, 2007.
ALBERTS, B.; JOHNSON, A.; LEWIS, J.; RAFF, M. ROBERTS, K.; WALTER, P. Molecular Biology of the cell 4th ed. New York: Garland Science, 2002.
ATEEQ, M. B.; FARAH, M. A.; ALI, N.; AHMAD, W. Induction of micronuclei and erythrocyte alterations in the catfish Clarias batrachus by 2,4-dichlorophenoxyacetic acid and butachlor. Mutation Res., v. 518, p. 135-144, 2002.
AU, D. W. T. The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar. Pollut. Bull., v. 48, p. 817-834, 2004.
AYAS, Z.; EKMEKCI, G.; OZMENB, M.; YERLI, S.V. Histopathological changes in the livers and kidneys of fish in Sariyar Reservoir, Turkey. Environ. Toxicol. Pharmacol., v. 23, p. 242-249, 2007.
AYLLON, F.; GARCIA-VAZQUEZ, E. Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: an assessment of the fish micronucleus test. Mutation Res., v. 467, p. 177-186, 2000.
BERNET, D.; SCHMIDT, H.; MEIER, W.; BURKHARDT-HOLM, P.; WAHLI, T. Histopathology in fish: proposal for a protocol to assess aquatic pollution. J. Fish. Dis., v. 22, p. 25-34, 1999.
BOENING, D. W. Ecological effects, transport, and fate of mercury: a general review. Chemosphere, v. 40, p. 1335-1351, 2000.
BOMBAIL, V.; AW, D.; GORDON, E.; BATTY, J. Application of the comet and micronucleus assay to butterfish (Pholis gunnellus) erythrocytes from the Firth of Forth, Scotland, Chemosphere, v. 44, p. 383-392, 2001.
BOON, J.P.; LEWIS,W.E.; CHOY, M.R.; ALLCHIN, C.R.; LAW R.J.; de BOER, J. Levels of polybrominated diphenyl ether (PBDE) flame retardants in animals representing different trophic levels of the North Sea food web. Environ. Sci. Technol.,v. 36, p. 4025-4032, 2002.
CARRASCO, K. R.; TILBURY, K. L.; MYERS, M. S. Assessment of the Piscine Micronucleus Test as an in situ Biological Indicator of Chemical Contaminant Effects. Can. J. Fish. aquat. Sci., v. 47, p. 2123-2136, 1990.
ÇAVAS, T.; GARANKO, N. N.; ARKHIPCHUK, V. V. Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem. Toxicol., v. 43, p. 569-574, 2005.
FIGUEIREDO, J. L.; MENEZES, N.A. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo, Museu de Zoologia da Universidade de São Paulo São Paulo: Museu de Zoologia da Universidade de São Paulo, 1978. 110 p,
FISK, A. T.; HOBSON, K. A.; NORSTROM, R. J. Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwater Polynya marine food web. Environ. Sci. Technol., v. 35, p. 732-738, 2001.
FUIMAN, L. A.; WERNER, R. G. Fishery Science: The unique contribution of early life stages. Oxford: Blackwell Science, 2002.
GRISOLIA, C. K.; STARLING, F. L. R. M. Micronuclei monitoring of fishes from Lake Paranoá, under influence of sewage treatment plant discharges. Mutation Res., v. 491, p. 39-44, 2001.
HAYASHI, M.; UEDA, T.; UYENO, K.; WADA, K.; KINAE, N.; SAOTOME, K.; TANAKA, N.; TAKAI, A.; SASAKI, Y. F.; ASANO, N.; SOFUNI, T.; OJIMA, Y. Development of genotoxicity assay systems that use aquatic or ganisms. Mutation Res., v. 399, p. 125-133, 1998.
HEATH, A. G. Water pollution and fish physiology 2ed. Florida: CRC Press, 1995. 384 p.
HEDDLE, J. A.; CIMINO, M. C.; HAYASHI, M.; ROMAGNA, M. D.; TUCKER, J. D.; VANPRAIS, P. H., McGREGOR, J. T. Micronuclei as a index citogenetic damage: past, presence and future. Environ. Mol. Mutagen., v. 18, p. 277-291, 1991.
AGOE, C. H. Responses at the tissue level: quatitative methods in histopathology applied to ecotoxicology. In: NEWMAN, M. C., JAGOE, C. H. (Ed.). Ecotoxicology: A hierarchial treatment New York: Lewis Publishers; CRC Press, 1996.
LYONS, B. P.; STENTIFORD, G. D.; GREN, M.; BIGNELL, J.; BATERMAN, K.; FEIST, S. W.; GOODSIR, F.; REYNOLDS, W. J.; THAIN, J. E. DNA adduct analysis and histopathological biomarkers in European flounder (Platichthys flesus) sampled from UK estuaries. Mutation Res., v. 522, p. 177-186, 2004.
LIVINGSTONE, D. R. Biotechnology and pollution monitoring: use of molecular biomarker in the aquatic environment. J. Chem. Technol. Biotechnol., v. 57, p. 195-211, 1993.
LIVINGSTONE, D. R. The fate of organic xenobiotics in aquatic ecossystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp. Biochem. Physiol., v. 120A, p. 43 - 49, 1998.
MELA, M.; RANDI, M.A.F.; VENTURA, D.F.; CARVALHO, C.E.V.; PELLETIER, E., OLIVEIRA RIBEIRO, C.A. Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias alabaricus Ecotoxicol. Environ. Saf., <doi:10.1016/j.ecoenv.2006.11.013>
MIRANDA, A. L.; ROCHE, H.; RANDI, M. A. F.; MENEZES, M. L.; OLIVEIRA RIBEIRO, C. A. Bioaccumulation of chlorinated pesticides and PCBs in the tropical freshwater fish Hoplias malabaricus: Histopathological, physiological, and immunological findings. Environ. Int., <doi:10.1016/j.envint.2008.02.004.
OLIVEIRA RIBEIRO, C. A.; VOLLAIRE, Y.; SANCHEZ-CHARDI, A.; ROCHE, H. Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat. Toxicol., v. 74, p. 53-69, 2005.
PORTO, J. I. R.; ARAÚJO, C S. O.; FELDBERG, E. Mutagenic effects of mercury pollution as revealed by micronucleus test on three Amazonian fish species. Environ. Res., v. 97, p. 287-292, 2005.
RABITTO, I. S.; ALVES COSTA, J. R. M.; SILVA DE ASSIS, H. C., PELLETIER, E.; AKAISHI, F. M.; ANJOS, A.; RANDI, M. A. F.; OLIVEIRA RIBEIRO, C. A. Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: Histopathological and biochemical findings. Ecotoxicol. Environ. Saf., v. 60, p. 147-156, 2005.
ROBERTS, R. J. Patologia de los peces Madrid: Mundi-Prensa, 1981. 366 p.
VALDEZ DOMINGOS, F. X.; AZEVEDO, M.; SILVA, M. D.; RANDI, M. A. F.; FREIRE, C. A.; SILVA DE ASSIS, H. C.; OLIVEIRA RIBEIRO, C. A. Multibiomarker assessment of three Brazilian estuaries using oysters as bioindicators. Environ. Res., v. 105, n. 3, p. 350-363, 2007.
WESTER, P.W.; VAN DER VEN, L.T.M.; VETHAAK, A.D., GRINWIS, G.C.M., VOS, J.G. Aquatic toxicology: opportunities for enhancement through histopathology. Environ. Toxicol. Pharmacol., v. 11, p. 289-295, 2002.

Publication Dates

Publication in this collection
11 Oct 2011
Date of issue
June 2011

History

Reviewed
12 July 2010
Received
19 Feb 2010
Accepted
11 Nov 2010

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] AKAISHI, F. M.; ST-JEAN, S. D.; BISHAY, F.; CLARKE, J.; RABITTO, I. S.; OLIVEIRA RIBEIRO, C.A. Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquat. Toxicol., v. 82, n. 1, p. 1-14, 2007.

[2] ALBERTS, B.; JOHNSON, A.; LEWIS, J.; RAFF, M. ROBERTS, K.; WALTER, P. Molecular Biology of the cell 4th ed. New York: Garland Science, 2002.

[3] ATEEQ, M. B.; FARAH, M. A.; ALI, N.; AHMAD, W. Induction of micronuclei and erythrocyte alterations in the catfish Clarias batrachus by 2,4-dichlorophenoxyacetic acid and butachlor. Mutation Res., v. 518, p. 135-144, 2002.

[4] AU, D. W. T. The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar. Pollut. Bull., v. 48, p. 817-834, 2004.

[5] AYAS, Z.; EKMEKCI, G.; OZMENB, M.; YERLI, S.V. Histopathological changes in the livers and kidneys of fish in Sariyar Reservoir, Turkey. Environ. Toxicol. Pharmacol., v. 23, p. 242-249, 2007.

[6] AYLLON, F.; GARCIA-VAZQUEZ, E. Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: an assessment of the fish micronucleus test. Mutation Res., v. 467, p. 177-186, 2000.

[7] BERNET, D.; SCHMIDT, H.; MEIER, W.; BURKHARDT-HOLM, P.; WAHLI, T. Histopathology in fish: proposal for a protocol to assess aquatic pollution. J. Fish. Dis., v. 22, p. 25-34, 1999.

[8] BOENING, D. W. Ecological effects, transport, and fate of mercury: a general review. Chemosphere, v. 40, p. 1335-1351, 2000.

[9] BOMBAIL, V.; AW, D.; GORDON, E.; BATTY, J. Application of the comet and micronucleus assay to butterfish (Pholis gunnellus) erythrocytes from the Firth of Forth, Scotland, Chemosphere, v. 44, p. 383-392, 2001.

[10] BOON, J.P.; LEWIS,W.E.; CHOY, M.R.; ALLCHIN, C.R.; LAW R.J.; de BOER, J. Levels of polybrominated diphenyl ether (PBDE) flame retardants in animals representing different trophic levels of the North Sea food web. Environ. Sci. Technol.,v. 36, p. 4025-4032, 2002.

[11] CARRASCO, K. R.; TILBURY, K. L.; MYERS, M. S. Assessment of the Piscine Micronucleus Test as an in situ Biological Indicator of Chemical Contaminant Effects. Can. J. Fish. aquat. Sci., v. 47, p. 2123-2136, 1990.

[12] ÇAVAS, T.; GARANKO, N. N.; ARKHIPCHUK, V. V. Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem. Toxicol., v. 43, p. 569-574, 2005.

[13] FIGUEIREDO, J. L.; MENEZES, N.A. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo, Museu de Zoologia da Universidade de São Paulo São Paulo: Museu de Zoologia da Universidade de São Paulo, 1978. 110 p,

[14] FISK, A. T.; HOBSON, K. A.; NORSTROM, R. J. Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwater Polynya marine food web. Environ. Sci. Technol., v. 35, p. 732-738, 2001.

[15] FUIMAN, L. A.; WERNER, R. G. Fishery Science: The unique contribution of early life stages. Oxford: Blackwell Science, 2002.

[16] GRISOLIA, C. K.; STARLING, F. L. R. M. Micronuclei monitoring of fishes from Lake Paranoá, under influence of sewage treatment plant discharges. Mutation Res., v. 491, p. 39-44, 2001.

[17] HAYASHI, M.; UEDA, T.; UYENO, K.; WADA, K.; KINAE, N.; SAOTOME, K.; TANAKA, N.; TAKAI, A.; SASAKI, Y. F.; ASANO, N.; SOFUNI, T.; OJIMA, Y. Development of genotoxicity assay systems that use aquatic or ganisms. Mutation Res., v. 399, p. 125-133, 1998.

[18] HEATH, A. G. Water pollution and fish physiology 2ed. Florida: CRC Press, 1995. 384 p.

[19] HEDDLE, J. A.; CIMINO, M. C.; HAYASHI, M.; ROMAGNA, M. D.; TUCKER, J. D.; VANPRAIS, P. H., McGREGOR, J. T. Micronuclei as a index citogenetic damage: past, presence and future. Environ. Mol. Mutagen., v. 18, p. 277-291, 1991.

[20] AGOE, C. H. Responses at the tissue level: quatitative methods in histopathology applied to ecotoxicology. In: NEWMAN, M. C., JAGOE, C. H. (Ed.). Ecotoxicology: A hierarchial treatment New York: Lewis Publishers; CRC Press, 1996.

[21] LYONS, B. P.; STENTIFORD, G. D.; GREN, M.; BIGNELL, J.; BATERMAN, K.; FEIST, S. W.; GOODSIR, F.; REYNOLDS, W. J.; THAIN, J. E. DNA adduct analysis and histopathological biomarkers in European flounder (Platichthys flesus) sampled from UK estuaries. Mutation Res., v. 522, p. 177-186, 2004.

[22] LIVINGSTONE, D. R. Biotechnology and pollution monitoring: use of molecular biomarker in the aquatic environment. J. Chem. Technol. Biotechnol., v. 57, p. 195-211, 1993.

[23] LIVINGSTONE, D. R. The fate of organic xenobiotics in aquatic ecossystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp. Biochem. Physiol., v. 120A, p. 43 - 49, 1998.

[24] MELA, M.; RANDI, M.A.F.; VENTURA, D.F.; CARVALHO, C.E.V.; PELLETIER, E., OLIVEIRA RIBEIRO, C.A. Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias alabaricus Ecotoxicol. Environ. Saf., <doi:10.1016/j.ecoenv.2006.11.013>

[25] MIRANDA, A. L.; ROCHE, H.; RANDI, M. A. F.; MENEZES, M. L.; OLIVEIRA RIBEIRO, C. A. Bioaccumulation of chlorinated pesticides and PCBs in the tropical freshwater fish Hoplias malabaricus: Histopathological, physiological, and immunological findings. Environ. Int., <doi:10.1016/j.envint.2008.02.004.

[26] OLIVEIRA RIBEIRO, C. A.; VOLLAIRE, Y.; SANCHEZ-CHARDI, A.; ROCHE, H. Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat. Toxicol., v. 74, p. 53-69, 2005.

[27] PORTO, J. I. R.; ARAÚJO, C S. O.; FELDBERG, E. Mutagenic effects of mercury pollution as revealed by micronucleus test on three Amazonian fish species. Environ. Res., v. 97, p. 287-292, 2005.

[28] RABITTO, I. S.; ALVES COSTA, J. R. M.; SILVA DE ASSIS, H. C., PELLETIER, E.; AKAISHI, F. M.; ANJOS, A.; RANDI, M. A. F.; OLIVEIRA RIBEIRO, C. A. Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: Histopathological and biochemical findings. Ecotoxicol. Environ. Saf., v. 60, p. 147-156, 2005.

[29] ROBERTS, R. J. Patologia de los peces Madrid: Mundi-Prensa, 1981. 366 p.

[30] VALDEZ DOMINGOS, F. X.; AZEVEDO, M.; SILVA, M. D.; RANDI, M. A. F.; FREIRE, C. A.; SILVA DE ASSIS, H. C.; OLIVEIRA RIBEIRO, C. A. Multibiomarker assessment of three Brazilian estuaries using oysters as bioindicators. Environ. Res., v. 105, n. 3, p. 350-363, 2007.

[31] WESTER, P.W.; VAN DER VEN, L.T.M.; VETHAAK, A.D., GRINWIS, G.C.M., VOS, J.G. Aquatic toxicology: opportunities for enhancement through histopathology. Environ. Toxicol. Pharmacol., v. 11, p. 289-295, 2002.