Comparison to Toxic Effects of Copper Oxide Nanoparticles and Copper Sulphate on Some Serum Parameters and Enzyme Activities of Oreochromis niloticus
Yıl 2021,
, 514 - 521, 31.12.2021
Mustafa Tunçsoy
,
Cahit Erdem
Öz
Today, human effects due to industrial development and population increase caused water ecosystems to be polluted by various pollutant such as heavy metals. Serum biochemical parameters are widely used in blood analysis and these parameters are suitable indicators for monitoring physiological changes in fish. Hence, the aim of present study to the effects of waterborne copper on serum glucose, total protein, albumin and triglyceride levels and serum cholinesterase (ChE), aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkalane phosphatase (ALP) and lactate dehydrogenase (LDH) activities of O. niloticus were determined after exposing the fish to 10, 50 and 100 µg/L copper applied as CuO nanoparticles (CuO NPs) and CuSO4 over 1, 7 and 15 days.
No mortality was observed during the experiments. Serum glucose and albumin levels increased while serum total protein, cholesterol and triglyceride levels decreased compared to control at the end of the 15th day. There was also a decrease in serum ChE activity whereas serum AST, ALT, ALP and LDH activities increased. Overall, CuSO4 and CuO NPs had similar effects in serum parameters of O. niloticus.
Destekleyen Kurum
University of Çukurova, Scientific Research Projects Coordination Unit and The Scientific and Technological Research Council of Turkey (TUBITAK)
Proje Numarası
(PhD Thesis, Project Number: FEF2013D45) and (TUBITAK Project Number: 1649B031402139)
Teşekkür
We also thanks to Prof.Dr. Maria João Bebianno, Asst.Prof.Dr. Margarida Ribau Teixeira, Dr. Tânia Gomes and Vânia Sousa.
Kaynakça
- Abdel-Daim, M.M., Eissa, I.A., Abdeen, A., Abdel-Latif, H.M., Ismail, M., Dawood, M.A. & Hassan, A.M. (2019). Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ. Toxicol. Pharmacol, 69:44-50.
- Abdel-Latif, H.M.R., Dawood, M.A.O., Mahmoud, S.F., Shukry, M., Noreldin, A.E., Ghetas, H.A. & Khallaf. M.A. (2021). Copper Oxide Nanoparticles Alter Serum Biochemical Indices, Induce Histopathological Alterations, and Modulate Transcription of Cytokines, HSP70, and Oxidative Stress Genes in Oreochromis niloticus. Animals, 11(3):652.
- Abdel-Khalek, A.A., Kadry, M.A.M., Badran, S.R. & Marie, M.S. (2015). Comparative Toxicity of Copper Oxide Bulk and Nano Particles in Nile Tilapia; Oreochromis niloticus: Biochemical and Oxidative Stress. J Basic Appl Biol, 72:43-57.
- Bhatt, I. & Tripathi, B.N. (2011). Interaction of Engineered Nanoparticles with Various Components of the Environment and Possible Strategies for Their Risk Assessment. Chemosphere 82(3):308-317.
- Brown, J.A. (1993). Endocrine Responses to Environmental Pollutants. In: Rankin, J.C., Jensen, F.B. (eds.) Fish Ecophysiology. Chapman and Hall, London, UK, s. 276-296.
- Buffet, P.E., Tankoua, O.F., Pan, J.F., Berhanu, D., Herrenknecht, C., Poirier, L., Amiard-Triquet, C., Amiard, J.C., Bérard, J.B., Risso, C., Guibbolini, M., Roméo, M., Reip, P., Valsami-Jones, E. & Mouneyrac, C. (2011). Behavioural and Biochemical Responses of Two Marine Invertebrates Scrobicularia plana and Hediste diversicolor to Copper Oxide Nanoparticles. Chemosphere 84:166-174.
- Bundschuh, M., Filser, J., Lüderwald, S., McKee, M.S., Metreveli, G., Schaumann, G.E., Schulz, R. & Wagner, S. (2018). Nanoparticles in the environment: where do we come from, where do we go to? Environ Sci Eur, 30(1):6.
- Chen, C.Y., Wooster, G.A. & Bowser, P.R. (2004). Comparative Blood Chemistry and Histopathology of Tilapia Infected with Vibrio vulnificus or Streptococcus iniae or Exposed to Carbon Tetrachloride, Gentamicin or Copper Sulphate. Aquac, 239:421-443.
- Cicik, B. & Engin, K. (2005). The Effects of Cadmium on Levels of Glucose in Serum and Glycogen Reserves in the Liver and Muscle Tissues of Cyprinus carpio (L., 1758). Turk J Vet Anim Sci, 29:113-117.
- De, T.K., De, M., Das, S., Ray, R. & Ghosh, P.B. (2010). Level of Heavy Metals in Some Edible Marine Fishes of Mangrove Dominated Tropical Estuarine Areas of Hooghly River, North East Coast of Bay of Bengal, India. Bull Environ Contam Toxicol, 85:385-390.
- Gomes, T., Pereira, C.G., Cardoso, C. & Bebianno, M.J. (2013). Differential Protein Expression in Mussels Mytilus galloprovincialis Exposed to Nano and Ionic Ag. Aquat Toxicol, 136(137):79-90.
- Heydarnejad, M.S., Khosravian-Hemami, M., Nematollahi, A. & Rahnama, S. (2013). Effects of Copper at Sublethal Concentrations on Growth and Biochemical Parameters in Rainbow Trout (Oncorhynchus mykiss). Int Rev Hydrobiol. 98:71-79.
- Hoseini, S.M., Hosseini, S.A. & Soudagar, M. (2012). Dietary Tryptophan Changes Serum Stress Markers, Enzyme Activity, and Ions Concentration of Wild Common Carp Cyprinus carpio Exposed to Ambient Copper. Fish Physiol Biochem, 38(5):1419-1426.
- Hoseini, S.M., Hedayati, A., Taheri Mirghaed, A. & Ghelichpour, M. (2016). Toxic Effects of Copper Sulfate and Copper Nanoparticles on Minerals, Enzymes, Thyroid Hormones and Protein Fractions of Plasma and Histopathology in Common Carp Cyprinus carpio. Experiment Toxicol Pathol, 68(9):493-503.
- Iwama, G.K., Vijayan, M.M., Forsyth, R.B. & Ackerman, P.A. (1999). Heat Shock Proteins and Physiological Stress in Fish. Am Zool, 39:901-909.
- Jiraungkoorskul, W., Upatham, E.S., Kruatrachue, M., Shaphong, S., Vichasri-Grams, S. & Pokethitiyook, P. (2003). Biochemical and Histopathological Effects of Glyphosate Herbicide on Nile Tilapia (Oreochromis niloticus). Environ Toxicol, 18:260-267.
- Ji, C.L., Wang, Q., Wu, H.F., Tan, Q.G. & Wang, W.X. (2015). A Metabolomic Investigation of the Effects of Metal Pollution in Oysters Crassostrea hongkongensis. Mar. Pollut. Bull, 90:21-222.
- Jorgensen, S.W. (2010). A Derivative of Encyclopedia of Ecology. In: Ecotoxicology. Academic Press, London, pp. 390.
- Karan, V., Vitorović, S., Tutundžić, V. & Poleksić, V. (1998). Functional Enzymes Activity and Gill Histology of Carp After Copper Sulfate Exposure and Recovery. Ecotoxicol Environ Safe, 40(1):49-55.
- Kaviani, E., Naeemi, A. & Salehzadeh, A. (2019). Influence of copper oxide nanoparticle on hematology and plasma bio-chemistry of Caspian trout (Salmo trutta caspius), following acute and chronic exposure. Poll, 5:225-234.
- Klaine, S.J., Alvarez, P.J.J., Batley, G.E., Fernandes, T.F., Handy, R.D., Lyon, D.Y., Mahendra, S., Mclaughlin, M.J. & Lead, J.R. (2008). Nanomaterials in The Environment: Behavior, Fate, Bioavailability and Effects. Environ Toxicol Chem, 27(9):1825-1851.
- Levesque, H.M., Moon, T.W., Campbell, P.G.C. & Hontela, A. (2002). Seasonal Variation in Carbohydrate and Lipid Metabolism of Yellow Perch (Perca flavescens) Chronically Exposed to Metals in the Field. Aquat Toxicol, 60:257-267.
- Mansouri, B., Maleki, A., Davari, B., Johari, S.A., Shahmoradi, B., Mohammadi, E. & Shahsavari, S. (2016). Histopathological Effects Following Short-Term Coexposure of Cyprinus carpio to Nanoparticles of TiO2 and CuO. Environ Monit Assess, 188(575):5-12.
- Mazandarini, M. & Hoseini, S.M. (2015). Anaemia and Plasma Lipid Profile in Common Carp (Cyprinus carpio) Exposed to Ambient Copper Sulphate and Nano-Scale Copper Oxide. Aquac Res, 1-9.
- Nel, A.E., Madler, L., Velegol, D., Xia, T., Hoek, E.M., Somasundaran, P., Klaessig, F., Castranova, V. & Thompson, M. (2009). Understanding Biophysiochemical Interactions at the Nanobio Interface. Nat Mater, 8:543-557.
- Nemcsok, J. & Hughes, G.M. (1988) The Effect of Copper Sulphate on Some Biochemical Parameters of Rainbow Trout. Environ Poll, 49:77-85.
- Newman, S.H., Piatt, J.F. & White, J. (1997). Hematological and Plasma Biochemical Reference Ranges of Alaskan Seabirds: Their Ecological Significance and Clinical importance. Colon Waterbirds, 20(3):492–504.
- Palandökenlier, E. & Kargın, F. (2019). The Effects of Zinc Oxide Nanoparticles and Zinc Sulphate on Some Biochemical Parameters in Blood Tissue of Oreochromis niloticus. Anatolian Env. and Anim. Sciences, 4(3), 447-453.
- Pretto, A., Loro, V.L., Silva, V.M.M., Salbego, J., de Menezes, C.C. & Souza, C.F. (2014). Exposure to Sublethal Concentrations of Copper Changes Biochemistry Parameters in Silver Catfish, Rhamdia quelen, (Quoy & Gaimard, 1824). Bull Environ Contam Toxicol, 392-399
- Ramesh, M., Senthil Kumaran, S., Kavith, C., Saravanan, M. & Mustafa, A. (2007). Primary Stress Responses of Common Carp, Cyprinus carpio Exposed to Copper Toxicity. Acta Ichthyol Piscat, 37:81-85.
- Ringwood, A.H., McCarthy, M., Bates, T.C. & Carroll, D.L. (2010). The Effects of Silver Nanoparticles on Oyster Embryos. Mar Environ Res, 69(1):549-551.
Tolaymat, T., El Badawy, A., Genaidy, A., Abdelraheem, W. & Sequeira, R. (2017). Analysis of metallic and metal oxide nanomaterial environmental emissions. J Clean Prod, 143:401-412.
- Tunçsoy, M., Duran, S., Yesilbudak, B., Ay, O., Cicik, B. & Erdem, C. (2016). Short Term Effects of Zinc on some Sera Biochemical Parameters and on Tissue Accumulation of Clarias gariepinus. Fresen Environ Bull, 25(2):658-664.
- Tunçsoy, M. & Erdem, C. (2018). Copper Accumulation in Tissues of Oreochromis niloticus Exposed to Copper Oxide Nanoparticles and Copper Sulphate with Their Effect on Antioxidant Enzyme Activities in Liver. Water Air Soil Poll, 229(269):1-10.
- Tunçsoy, M. & Duran, S. (2020). Acute Toxicity of Titanium Dioxide Nanoparticles on Some Serum Parameters and Enzyme Activities of Cyprinus carpio. J. Anatolian Env. and Anim. Sciences 5(4):704-710.
- Tunçsoy, M. (2021). Impacts of Titanium Dioxide Nanoparticles on Serum Parameters and Enzyme Activities of Clarias gariepinus. Bull Environ Contam Toxicol, 106(4): 629-636.
- Vosyliene, M.Z. (1999). The Effect of Heavy Metals on Hematological Indices. Acta Zool Litv Hydrobiol, 9:76-82.
- Wang, S.L., Xu, X.R., Sun, Y.X., Liu, J.L. & Li, H.B. (2013). Heavy Metal Pollution in Coastal Areas of South China: A Review. Mar Pollut Bull, 76(1-2):7-15.
- Yang, J.L. & Chen, H.C. (2003). Effects of Gallium on Common Carp (Cyprinus carpio): Acute Test, Serum Biochemistry, and Erythrocyte Morphology. Chemosphere, 53:877-882.
Bakır oksit nanopartikülleri ve Bakır sülfatın O. niloticus’da Serum Parametreleri ve Serum Enzim Aktiviteleri Üzerine Toksik Etkilerinin Karşılaştırılması
Yıl 2021,
, 514 - 521, 31.12.2021
Mustafa Tunçsoy
,
Cahit Erdem
Öz
Günümüzde endüstriyel gelişmeler ve nüfus artışına bağlı insan etkileri su ekosistemlerinin ağır metaller gibi çeşitli kirleticiler tarafından kirletilmesine neden olmuştur. Serum biyokimyasal parametreleri kan analizinde yaygın olarak kullanılmaktadır ve bu parametreler balıklarda fizyolojik değişikliklerin izlenmesi için uygun belirteçlerdir. Bu çalışmada 10, 50 ve 100 µg/L CuO nanopartikülleri (CuO NP) ve bakır sülfatın (CuSO4) 1, 7 ve 15 günlük sürelerle etkisinde O. niloticus’ da serum glikoz, total protein, albumin, kolesterol ve trigliserit düzeyleri ile serum ChE, AST, ALT, ALP ve LDH enzim aktivitelerinin belirlenmesi amaçlanmıştır.
Deney süresince tüm derişimlerde herhangi bir mortalite gözlenmemiştir. 15 günlük deney süresi sonunda her iki ugulamada da serum glikoz ve albümin düzeyleri artış gösterirken, serum total protein, kolesterol ve trigliserit düzeylerinde azalış gösterdiği belirlenmiştir. Serum enzim aktivitelerinde ise ChE aktivitesi azalma gösterirken, serum AST, ALT, ALP ve LDH aktiviteleri deney süresi sonunda artış göstermiştir. Sonuç olarak O. niloticus serum parametreleri üzerine toksik etkileri karşılaştırıldığında her iki uygulamanın da benzer etkiler gösterdiği belirlenmiştir.
Proje Numarası
(PhD Thesis, Project Number: FEF2013D45) and (TUBITAK Project Number: 1649B031402139)
Kaynakça
- Abdel-Daim, M.M., Eissa, I.A., Abdeen, A., Abdel-Latif, H.M., Ismail, M., Dawood, M.A. & Hassan, A.M. (2019). Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ. Toxicol. Pharmacol, 69:44-50.
- Abdel-Latif, H.M.R., Dawood, M.A.O., Mahmoud, S.F., Shukry, M., Noreldin, A.E., Ghetas, H.A. & Khallaf. M.A. (2021). Copper Oxide Nanoparticles Alter Serum Biochemical Indices, Induce Histopathological Alterations, and Modulate Transcription of Cytokines, HSP70, and Oxidative Stress Genes in Oreochromis niloticus. Animals, 11(3):652.
- Abdel-Khalek, A.A., Kadry, M.A.M., Badran, S.R. & Marie, M.S. (2015). Comparative Toxicity of Copper Oxide Bulk and Nano Particles in Nile Tilapia; Oreochromis niloticus: Biochemical and Oxidative Stress. J Basic Appl Biol, 72:43-57.
- Bhatt, I. & Tripathi, B.N. (2011). Interaction of Engineered Nanoparticles with Various Components of the Environment and Possible Strategies for Their Risk Assessment. Chemosphere 82(3):308-317.
- Brown, J.A. (1993). Endocrine Responses to Environmental Pollutants. In: Rankin, J.C., Jensen, F.B. (eds.) Fish Ecophysiology. Chapman and Hall, London, UK, s. 276-296.
- Buffet, P.E., Tankoua, O.F., Pan, J.F., Berhanu, D., Herrenknecht, C., Poirier, L., Amiard-Triquet, C., Amiard, J.C., Bérard, J.B., Risso, C., Guibbolini, M., Roméo, M., Reip, P., Valsami-Jones, E. & Mouneyrac, C. (2011). Behavioural and Biochemical Responses of Two Marine Invertebrates Scrobicularia plana and Hediste diversicolor to Copper Oxide Nanoparticles. Chemosphere 84:166-174.
- Bundschuh, M., Filser, J., Lüderwald, S., McKee, M.S., Metreveli, G., Schaumann, G.E., Schulz, R. & Wagner, S. (2018). Nanoparticles in the environment: where do we come from, where do we go to? Environ Sci Eur, 30(1):6.
- Chen, C.Y., Wooster, G.A. & Bowser, P.R. (2004). Comparative Blood Chemistry and Histopathology of Tilapia Infected with Vibrio vulnificus or Streptococcus iniae or Exposed to Carbon Tetrachloride, Gentamicin or Copper Sulphate. Aquac, 239:421-443.
- Cicik, B. & Engin, K. (2005). The Effects of Cadmium on Levels of Glucose in Serum and Glycogen Reserves in the Liver and Muscle Tissues of Cyprinus carpio (L., 1758). Turk J Vet Anim Sci, 29:113-117.
- De, T.K., De, M., Das, S., Ray, R. & Ghosh, P.B. (2010). Level of Heavy Metals in Some Edible Marine Fishes of Mangrove Dominated Tropical Estuarine Areas of Hooghly River, North East Coast of Bay of Bengal, India. Bull Environ Contam Toxicol, 85:385-390.
- Gomes, T., Pereira, C.G., Cardoso, C. & Bebianno, M.J. (2013). Differential Protein Expression in Mussels Mytilus galloprovincialis Exposed to Nano and Ionic Ag. Aquat Toxicol, 136(137):79-90.
- Heydarnejad, M.S., Khosravian-Hemami, M., Nematollahi, A. & Rahnama, S. (2013). Effects of Copper at Sublethal Concentrations on Growth and Biochemical Parameters in Rainbow Trout (Oncorhynchus mykiss). Int Rev Hydrobiol. 98:71-79.
- Hoseini, S.M., Hosseini, S.A. & Soudagar, M. (2012). Dietary Tryptophan Changes Serum Stress Markers, Enzyme Activity, and Ions Concentration of Wild Common Carp Cyprinus carpio Exposed to Ambient Copper. Fish Physiol Biochem, 38(5):1419-1426.
- Hoseini, S.M., Hedayati, A., Taheri Mirghaed, A. & Ghelichpour, M. (2016). Toxic Effects of Copper Sulfate and Copper Nanoparticles on Minerals, Enzymes, Thyroid Hormones and Protein Fractions of Plasma and Histopathology in Common Carp Cyprinus carpio. Experiment Toxicol Pathol, 68(9):493-503.
- Iwama, G.K., Vijayan, M.M., Forsyth, R.B. & Ackerman, P.A. (1999). Heat Shock Proteins and Physiological Stress in Fish. Am Zool, 39:901-909.
- Jiraungkoorskul, W., Upatham, E.S., Kruatrachue, M., Shaphong, S., Vichasri-Grams, S. & Pokethitiyook, P. (2003). Biochemical and Histopathological Effects of Glyphosate Herbicide on Nile Tilapia (Oreochromis niloticus). Environ Toxicol, 18:260-267.
- Ji, C.L., Wang, Q., Wu, H.F., Tan, Q.G. & Wang, W.X. (2015). A Metabolomic Investigation of the Effects of Metal Pollution in Oysters Crassostrea hongkongensis. Mar. Pollut. Bull, 90:21-222.
- Jorgensen, S.W. (2010). A Derivative of Encyclopedia of Ecology. In: Ecotoxicology. Academic Press, London, pp. 390.
- Karan, V., Vitorović, S., Tutundžić, V. & Poleksić, V. (1998). Functional Enzymes Activity and Gill Histology of Carp After Copper Sulfate Exposure and Recovery. Ecotoxicol Environ Safe, 40(1):49-55.
- Kaviani, E., Naeemi, A. & Salehzadeh, A. (2019). Influence of copper oxide nanoparticle on hematology and plasma bio-chemistry of Caspian trout (Salmo trutta caspius), following acute and chronic exposure. Poll, 5:225-234.
- Klaine, S.J., Alvarez, P.J.J., Batley, G.E., Fernandes, T.F., Handy, R.D., Lyon, D.Y., Mahendra, S., Mclaughlin, M.J. & Lead, J.R. (2008). Nanomaterials in The Environment: Behavior, Fate, Bioavailability and Effects. Environ Toxicol Chem, 27(9):1825-1851.
- Levesque, H.M., Moon, T.W., Campbell, P.G.C. & Hontela, A. (2002). Seasonal Variation in Carbohydrate and Lipid Metabolism of Yellow Perch (Perca flavescens) Chronically Exposed to Metals in the Field. Aquat Toxicol, 60:257-267.
- Mansouri, B., Maleki, A., Davari, B., Johari, S.A., Shahmoradi, B., Mohammadi, E. & Shahsavari, S. (2016). Histopathological Effects Following Short-Term Coexposure of Cyprinus carpio to Nanoparticles of TiO2 and CuO. Environ Monit Assess, 188(575):5-12.
- Mazandarini, M. & Hoseini, S.M. (2015). Anaemia and Plasma Lipid Profile in Common Carp (Cyprinus carpio) Exposed to Ambient Copper Sulphate and Nano-Scale Copper Oxide. Aquac Res, 1-9.
- Nel, A.E., Madler, L., Velegol, D., Xia, T., Hoek, E.M., Somasundaran, P., Klaessig, F., Castranova, V. & Thompson, M. (2009). Understanding Biophysiochemical Interactions at the Nanobio Interface. Nat Mater, 8:543-557.
- Nemcsok, J. & Hughes, G.M. (1988) The Effect of Copper Sulphate on Some Biochemical Parameters of Rainbow Trout. Environ Poll, 49:77-85.
- Newman, S.H., Piatt, J.F. & White, J. (1997). Hematological and Plasma Biochemical Reference Ranges of Alaskan Seabirds: Their Ecological Significance and Clinical importance. Colon Waterbirds, 20(3):492–504.
- Palandökenlier, E. & Kargın, F. (2019). The Effects of Zinc Oxide Nanoparticles and Zinc Sulphate on Some Biochemical Parameters in Blood Tissue of Oreochromis niloticus. Anatolian Env. and Anim. Sciences, 4(3), 447-453.
- Pretto, A., Loro, V.L., Silva, V.M.M., Salbego, J., de Menezes, C.C. & Souza, C.F. (2014). Exposure to Sublethal Concentrations of Copper Changes Biochemistry Parameters in Silver Catfish, Rhamdia quelen, (Quoy & Gaimard, 1824). Bull Environ Contam Toxicol, 392-399
- Ramesh, M., Senthil Kumaran, S., Kavith, C., Saravanan, M. & Mustafa, A. (2007). Primary Stress Responses of Common Carp, Cyprinus carpio Exposed to Copper Toxicity. Acta Ichthyol Piscat, 37:81-85.
- Ringwood, A.H., McCarthy, M., Bates, T.C. & Carroll, D.L. (2010). The Effects of Silver Nanoparticles on Oyster Embryos. Mar Environ Res, 69(1):549-551.
Tolaymat, T., El Badawy, A., Genaidy, A., Abdelraheem, W. & Sequeira, R. (2017). Analysis of metallic and metal oxide nanomaterial environmental emissions. J Clean Prod, 143:401-412.
- Tunçsoy, M., Duran, S., Yesilbudak, B., Ay, O., Cicik, B. & Erdem, C. (2016). Short Term Effects of Zinc on some Sera Biochemical Parameters and on Tissue Accumulation of Clarias gariepinus. Fresen Environ Bull, 25(2):658-664.
- Tunçsoy, M. & Erdem, C. (2018). Copper Accumulation in Tissues of Oreochromis niloticus Exposed to Copper Oxide Nanoparticles and Copper Sulphate with Their Effect on Antioxidant Enzyme Activities in Liver. Water Air Soil Poll, 229(269):1-10.
- Tunçsoy, M. & Duran, S. (2020). Acute Toxicity of Titanium Dioxide Nanoparticles on Some Serum Parameters and Enzyme Activities of Cyprinus carpio. J. Anatolian Env. and Anim. Sciences 5(4):704-710.
- Tunçsoy, M. (2021). Impacts of Titanium Dioxide Nanoparticles on Serum Parameters and Enzyme Activities of Clarias gariepinus. Bull Environ Contam Toxicol, 106(4): 629-636.
- Vosyliene, M.Z. (1999). The Effect of Heavy Metals on Hematological Indices. Acta Zool Litv Hydrobiol, 9:76-82.
- Wang, S.L., Xu, X.R., Sun, Y.X., Liu, J.L. & Li, H.B. (2013). Heavy Metal Pollution in Coastal Areas of South China: A Review. Mar Pollut Bull, 76(1-2):7-15.
- Yang, J.L. & Chen, H.C. (2003). Effects of Gallium on Common Carp (Cyprinus carpio): Acute Test, Serum Biochemistry, and Erythrocyte Morphology. Chemosphere, 53:877-882.