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Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria

Year 2014, Volume: 14 Issue: 1, - , 07.07.2014
https://doi.org/10.4194/1303-2712-v14_1_23

Abstract

Lake Karla, Greece, is a partially reconstructed lake. The lake's water filling process started in September 2009. Existing evidence based on the prevailing microorganisms and cyanotoxin levels in the lake in 2010 suggested that the lake could have a negative effect on its biota. By investigating whether Carassius gibelio individuals bear brain and liver histopathological findings, this study complements the data now available from the first year of L. Karla's reconstruction. Based on the 16S rRNA gene diversity, the potentially toxic cyanobacteria Anabaenopsis sp. and Planktothrix were shown to be present in the lake's water in May 2011. C. gibelio specimens were collected a month later. Histopathological alterations in the liver of the individuals, namely picnotic nuclei, loss of structure and hemorrhagic regions, were detected by microscopic examination. Picnotic nuclei, loss of the liver structure and hemorrhagic regions were detected. These alterations may be associated with the occurrence of cyanobacterial toxins possibly produced by the potentially toxic cyanobacterial species found in the water column. No alterations were found in the brain, probably due to the existence of the blood-brain barrier.

References

  • Closest known relative KRL3-AM1 5% Clone LiUU-11-276 (100%) (HQ386368) Lake water GENBANK , unpublished Anabaenopsis nadsonii (100%) (FM177482)
  • KRL3-AM2 4% Oscillatoria sp. (99%) (AJ133106) Lake water GENBANK , unpublished _ KRL3AM19 4% Clone NV1_CYA_1_2 (99%) (FJ204888) Lake water GENBANK , unpublished Mastigocladopsis sp. (89%) (DQ235802) KRL3AM11 3,1% Clone SSW9Ap (98%) (EU592382) Brackish waters Dillon et al. (2009) Limnothrix sp. (92%) (AF212922) KRL3AM14 1% Symphyonemopsis sp. (98%) (AJ544085) Cave Gügger et al (2004) _ KRL3AM33 1% Clone 4550-27F (99%) (FR648052) Sea water Sjostedt et al. (2012) Synechococcus sp. (98%) (AY151238)
  • KRL3-AM6 1% Clone 2S8 (99%) (GU074287) Freshwater AizenbergGershtein et al. (2012) _
  • Figure 1. Histological sections of Carassius gibelio’s brain. A. The brain tissue showed normal histological architect without any indication of deformities. B. No erythrocytes were detected in the outer space of the brain blood vessels (arrows). Bar=100 μm. a thickness of three or more cells were noted. It can be signs of indicative hyperplasia or a possible early stage neoplasia. Hepatocytes contained large cytoplasmic vacuoles (clear regions in hepatocyte cytoplasm), while the portal tracks appeared to be normal without cirrhosis signs. Liver observation under the scanning electron microscope revealed damage to many of the cells’ plasma membranes (Figure 3), which appeared to be broken and punctured on their surface (Figure 3). These cells can be described as necrotic cells. Discussion Lake Karla is already known to host intense cynobacterial blooms, and the toxins produced have been found in Cyprinus carpio tissues (Papadimitriou et al., 2013). For this reason, in this study we aimed at investigating whether there were any histopathological findings in another fish species existing in the lake, i.e. Carassius gibelio. At the same time, we confirmed the existence of potentially toxic cyanobacterial species by 16S rRNA gene diversity and measurement of MCYSTs concentrations, already known to prevail in the lake
  • (Papadimitriou et al., 2013). A MCYSTs level of 20 μg MCYST-LR /L represents a guideline value for a moderate health risk in recreational waters (WHO, 1998). This concentration is equivalent to 100,000 cyanobacterial cells per ml, or approximately 50 μg/L chlorophyll-a if cyanobacteria, and especially Microcystis sp. dominate. It is 20 times higher than the WHO provisional Guideline Value concentration for microcystin- LR drinking water of 1 μg/L (WHO, 1998). MCYSTs values for Lake Karla (Table 2) were below the WHO Guide level for recreational waters, but much higher than the WHO Guide level for drinking water.
  • The water and seston MCYSTs concentrations, along with the existence of the two potentially toxic cyanobacterial phylotypes, raised two questions: a) whether Carassius gibelio individuals of the lake were affected and b) if yes, in what capacity? C. gibelio is a member of the family Cyprinidae. It is not a widely commercial fish, but is consumed in many regions of Greece. It is omnivorous; feeding on plankton, zoobenthos, invertebrates, plant material, and detritus (Specziár et al., 1997; 1998; Kottelat and Freyhof, 2007). However, as a result to its method of water filtration in order to obtain its main food source, large quantities of filamentous and colonial cyanobacteria often occur in its digestive tract (Kolmakov and Gladyshev, 2003). MCYSTs Ananiadis, C.I. 1959. Limnological study of Lake Karla. Bulletin de l’Institut Oc´eanographique, 1083: 1–19.
  • Bartram, J., Burch, M., Falconer, I.R., Jones, G. and Kuiper-Goodman, T. 1999. Situation assessment, planning and management. In: I. Chorus, J. Bartram (Eds), Toxic cyanobacteria in water, Taylor and Francis, London, New York: 179-209.
  • Carbis, C.R., Rawlin, G.T., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1996. The histopathology of carp, Cyprinus carpio L., exposed to microcystins by gavage, immersion and intraperitoneal administration. Journal of Fish Diseases, 19: 199–207. doi: 1111/j.1365-2761.1996.tb00126.x
  • Carbis, C.R., Rawlin, G.T., Grant, P., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1997. A study of feral carp, Cyprinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health. Journal of Fish Diseases, 20: 81–91. doi: 10.1046/j.1365-2761.1997.d01-111.x Carmichael, W.W., Azevedo, S.M.F.O., An, J.S., Molica, R.J., Jochimsen, E.M., Lau, S., Rinehart, K.L., Shaw, G.R. and Eaglesham, G.K. 2001. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environmental Health Perspectives, 109: 663-668. doi: 10.1289/ehp.01109663
  • Chatzinikolaou, Y., Ioannou, A. and Lazaridou, M. 2010. Intrabasin spatial approach on pollution load estimation in a large Mediterranean river. Desalination, 250: 118–129. doi: 1016/j.desal.2008.12.062.
  • Chorus, I. 2001. Cyanotoxin occurrence in freshwaters-a summary of survey results from different countries. In: I. Chorus (Ed.), Cyanotoxins: Occurrence, causes consequences, Spinger, Berlin: 75-78.
  • Codd, G.A. 1995. Cyanobacterial toxins: occurrence, properties and biological significance. Water Science and Technology, 32(4): 149-156. doi: 10.1016/02731223(95)00692-3.
  • Codd, G.A., Chorus, I and Burch, M. 1999. Design of monitoring programmes. In: I. Chorus, J. Bartram (Eds), Toxic Cyanobacteria in water: a guide to their public health consequences, monitoring and management, E & FN Spon, London: 313-328.
  • Cooley, H.M., Evans, R.E. and Klaverkamp, J.F. 2000. Toxicology of dietary uranium in lake whitefish (Coregonus clupeaformis). Aquatic Toxicology, 48: 495–515. doi: 10.1016/S0166-445X(99)00057-0.
  • Dietrich, D. and Hoeger, S. 2005. Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? Toxicology and Applied Pharmacology, 203: 273–289. doi: 1016/j.taap.2004.09.005.
  • Dos Santos, A.P.M.E. and Bracarense, A.P.F.R.L. 2008. Hepatotoxicity associated with microcystins. Semina:Ciencias Agrarias, 29: 4174 doi: 10.5433/1679-0359.2008v29n2p417
  • Ernst, B. 2008. Investigations of the impact of toxic cyanobacteria on fish. PhD thesis, Constance, Germany: Universität Konstanz. Dissertation, University of Kostanz.
  • Fisher, W., Dietrich, D. 2000a. Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicology and Applied Pharmacology, 164: 73– doi: 10.1006/taap.1999.8861.
  • Fischer, W. and Dietrich, D. 2000b. Toxicity of the cyanobacterial cyclic heptapeptide toxins microcystin LR and-RR in early life-stages of the African clawed frog (Xenopus laevis). Aquatic Toxicology, 49: 189– 1 doi: 10.1016/S0166-445X(99)00079-X.
  • Fournie, J. W., Courtney, L.A. 2002. Histopathological evidence of regeneration following hepatotoxic effects of the cyanotoxin Microcystin-LR in the hardhead catfish and Gulf killifish. Journal of Aquatic Animal Health, 14: 273doi: 1577/15488667(2002)014<0273:HEORFH>2.0.CO;2.
  • Hawkins, B.T. and Davis, T.P. 2005. The blood-brain barrier/neurovascular unit in health and disease. Pharmacological Reviews, 57: 173-85. doi: 1124/pr.57.2.4.
  • Huisman, J., Matthijs, H.C.P. and Visser, P.M. 2005. Harmful cyanobacteria. Springer, Berlin, 243 pp.
  • Kagalou, I., Kormas, K.A., Papadimitriou, T., Katsiapi, M., Genitsaris, S. and Moustaka-Gouni, M. 2012. Greece: occurrence, monitoring and risk management of cyanobacteria and cyanotoxins. In: I. Chorus (Ed), Current approaches to cyanotoxin risk assessment, risk management and regulations in different countries, Federal Environmental Agency (Umweltbundesamt), Berlin: 71-78.
  • Kagalou, I., Papadimitriou, T., Bacopoulos, V. and Leonardos, I. 2008. Assessment of microcystins in lake water and the omnivorous fish (Carassius gibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environmental Monitoring and Assessment, 137: 185-195. doi: 1007/s10661-007-9739-6.
  • Katsiapi, M., Moustaka-Gouni, M., Vardaka, E. and Kormas, K.A. 20 Different phytoplankton descriptors show asynchronous changes in a shallow urban lake (L. Kastoria, Greece) after sewage diversion. Fundamental and Applied Limnology, 182:219-230. doi: 10.1127/1863-9135/2013/0362
  • Kolmakov, V. and Gladyshev, M. 2003. Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crusian carp. Aquatic Ecology, 37: 237-2 doi: 1023/A:1025801326088.
  • Kormas, K.A., Gkelis, S., Vardaka, E., Moustaka-Gouni, M. 20 Morphologic and molecular analysis of bloomforming Cyanobacteria in two eutrophic, shallow Mediterranean lakes. Limnologica, 41: 167-173. doi: 1016/j.limno.2010.10.003.
  • Kotak, B.J., Semalulu, S., Friytz, D.L., Prepas, E.E., Hrudey, S.E., Coppock, R.W. 1996. Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). Toxicon, 34: 517–25. doi: 10.1016/00410101(96)00009-8.
  • Kottelat, M. and Freyhof, J. 2007. Handbook of European freshwater fishes. Publications Kottelat, Berlin, 646 pp.
  • Lang, T., Wosniok, W., Barsiene, J., Broeg, K., Kopecka, J. and Parkkonen, J. 2006. Liver histopathology in Baltic flounder (Platichthys flesus) as indicator of biological effects of contaminants. Marine Pollution Bulletin, 53: 488-4 doi: 1016/j.marpolbul.2005.11.008.
  • Li, L., Xie, P., Li, S., Qiu, T., Guo, L. 2007. Sequential ultrastructural and biochemical changes induced in vivo by the hepatotoxic microcystins in liver of the phytoplanktivorous silver carp Hypophthalmichthys molitrix. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146: 357–367. doi: 1016/j.cbpc.2007.04.008.
  • Malbrouck, C., Kestemont, P. 2006. Effects of Microcystins on fish. Environmental Toxicology and Chemistry, 25: 72–86. doi: 10.1897/05-029R.1.
  • Mitsoura, A., Kagalou, I., Papaioannou, N., Berillis, P., Mente, E. and Papadimitriou T. 2013. The presence of microcystins in fish Cyprinus carpio tissues: an histopathological study. International Aquatic Research, 5: 8. doi:10.1186/2008-6970-5-8
  • Moutou, K., Tsikogias, S., Papadimitriou, T. and Kagalou, I. 2012. Oxidative stress in Cyprinus carpio to analyze microcystin impact in eutrophic shallow lakes: a preliminary study. Journal of Enviromental Monitoring, 14(8): 2195-2203. doi: 1039/c2em30129f.
  • Nikouli, E., Kormas, K.A., Berillis, P., Karayanni, H. and Moustaka-Gouni, M. 2013. Harmful and parasitic unicellular eukaryotes persist in a shallow lake under reconstruction (L. Karla, Greece). Hydrobiologia, 718: 73-83.
  • Nübel, U., Garcia-Pichel, F. and Muyzer, G. 1997. PCR primers to amplify 16S rRNA genes from Cyanobacteria. Applied and Environmental Microbiology, 63: 3327-3332.
  • Oikonomou, A., Κatsiapi, M., Karayanni, H., MoustakaGouni, M. and Kormas, K. 2012. Plankton microorganisms coinciding with two consecutive mass fish kills in a newly reconstructed lake. The Scientific World Journal. doi:10.1100/2012/504135.
  • Papadimitriou, T., Kagalou, I., Stalikas, C., Pilidis, G. and Leonardos, I. 2012. Assessment of microcystins distribution and biomagnification in tissues of the aquatic food web compartments from a shallow lake and potential risks for public health. Ecotoxicology, 21: 1155-1166. doi: 10.1007/s10646-012-0870-y.
  • Papadimitriou, T., Katsiapi, M., Kormas, K.A., MoustakaGouni, M. and Kagalou, I. 2013. Artificially-born "killer" lake: phytoplankton based water quality and microcystin affected fish in a reconstructed lake. Science of the Total Environment, 452-453:116-124. doi: 1016/j.scitotenv.2013.02.035.
  • Råbergh, C.M.I., Bylund, G. and Eriksson, J.E. 1991. Histopathological effects of microcystin-LR, a cyclic peptide toxin from the cyanobacterium (blue-green algae) Microcystis aeruginosa, on common carp (Cyprinus carpio L.). Aquatic Toxicology, 20: 131– doi: 10.1016/0166-445X(91)90012-X.
  • Specziár, A., Tölg, L. and Biró, P. 1997. Feeding strategy and growth of cyprinids in the littoral zone of Lake Balaton. Journal of Fish Biology, 51: 1109-1124. doi: 1006/jfbi.1997.0514.
  • Specziár, A., Biro, P. and Tolg, L. 1998. Feeding and competition of five cyprinid fishes in different habitats of the Lake Balaton littoral zone, Hungary. Italian Journal of Zoology, 65: 331-336. doi: 1080/11250009809386842.
  • Vardaka, E., Moustaka-Gouni, M., Cook, C.M. and Lanaras, T. 2005. Cyanobacterial blooms and water quality in Greek waterbodies. Journal of Applied Phycology, 17: 391-401. doi: 10.1007/s10811-0058700Welker, M., Chorus, I. and Fastner, J. 2004. Occurrence of cyanobacterial toxins (microcystins) in surface waters of rural Bangladesh- pilot study. In W.H.O. Report, Bangladesh: 1-24.
  • WHO 1998. Blue-green algae in inland waters: Assessment and control of risks to public health. WHO Document, Annex G.
  • Xie, L.Q., Xie, P., Ozawa, K., Honma, T., Yokoyama, A., and Park, H.D. 2004. Dynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environmental Pollution, 127: 431–439. doi: 1016/j.envpol.2003.08.011.
  • Zurawell, R.W., Chen, H., Burke, J.M. and Prepas, B.R. 200 Hepatotoxic cyanobacteria: A review of the biological importance of microcystins in freshwater environment. Journal of Toxicology and Environmental Health, 8(B): 1–37. doi: 1080/10937400590889412.

Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria

Year 2014, Volume: 14 Issue: 1, - , 07.07.2014
https://doi.org/10.4194/1303-2712-v14_1_23

Abstract

Lake Karla, Greece, is a partially reconstructed lake. The lake's water filling process started in September 2009. Existing evidence based on the prevailing microorganisms and cyanotoxin levels in the lake in 2010 suggested that the lake could have a negative effect on its biota. By investigating whether Carassius gibelio individuals bear brain and liver histopathological findings, this study complements the data now available from the first year of L. Karla's reconstruction. Based on the 16S rRNA gene diversity, the potentially toxic cyanobacteria Anabaenopsis sp. and Planktothrix were shown to be present in the lake's water in May 2011. C. gibelio specimens were collected a month later. Histopathological alterations in the liver of the individuals, namely picnotic nuclei, loss of structure and hemorrhagic regions, were detected by microscopic examination. Picnotic nuclei, loss of the liver structure and hemorrhagic regions were detected. These alterations may be associated with the occurrence of cyanobacterial toxins possibly produced by the potentially toxic cyanobacterial species found in the water column. No alterations were found in the brain, probably due to the existence of the blood-brain barrier.

References

  • Closest known relative KRL3-AM1 5% Clone LiUU-11-276 (100%) (HQ386368) Lake water GENBANK , unpublished Anabaenopsis nadsonii (100%) (FM177482)
  • KRL3-AM2 4% Oscillatoria sp. (99%) (AJ133106) Lake water GENBANK , unpublished _ KRL3AM19 4% Clone NV1_CYA_1_2 (99%) (FJ204888) Lake water GENBANK , unpublished Mastigocladopsis sp. (89%) (DQ235802) KRL3AM11 3,1% Clone SSW9Ap (98%) (EU592382) Brackish waters Dillon et al. (2009) Limnothrix sp. (92%) (AF212922) KRL3AM14 1% Symphyonemopsis sp. (98%) (AJ544085) Cave Gügger et al (2004) _ KRL3AM33 1% Clone 4550-27F (99%) (FR648052) Sea water Sjostedt et al. (2012) Synechococcus sp. (98%) (AY151238)
  • KRL3-AM6 1% Clone 2S8 (99%) (GU074287) Freshwater AizenbergGershtein et al. (2012) _
  • Figure 1. Histological sections of Carassius gibelio’s brain. A. The brain tissue showed normal histological architect without any indication of deformities. B. No erythrocytes were detected in the outer space of the brain blood vessels (arrows). Bar=100 μm. a thickness of three or more cells were noted. It can be signs of indicative hyperplasia or a possible early stage neoplasia. Hepatocytes contained large cytoplasmic vacuoles (clear regions in hepatocyte cytoplasm), while the portal tracks appeared to be normal without cirrhosis signs. Liver observation under the scanning electron microscope revealed damage to many of the cells’ plasma membranes (Figure 3), which appeared to be broken and punctured on their surface (Figure 3). These cells can be described as necrotic cells. Discussion Lake Karla is already known to host intense cynobacterial blooms, and the toxins produced have been found in Cyprinus carpio tissues (Papadimitriou et al., 2013). For this reason, in this study we aimed at investigating whether there were any histopathological findings in another fish species existing in the lake, i.e. Carassius gibelio. At the same time, we confirmed the existence of potentially toxic cyanobacterial species by 16S rRNA gene diversity and measurement of MCYSTs concentrations, already known to prevail in the lake
  • (Papadimitriou et al., 2013). A MCYSTs level of 20 μg MCYST-LR /L represents a guideline value for a moderate health risk in recreational waters (WHO, 1998). This concentration is equivalent to 100,000 cyanobacterial cells per ml, or approximately 50 μg/L chlorophyll-a if cyanobacteria, and especially Microcystis sp. dominate. It is 20 times higher than the WHO provisional Guideline Value concentration for microcystin- LR drinking water of 1 μg/L (WHO, 1998). MCYSTs values for Lake Karla (Table 2) were below the WHO Guide level for recreational waters, but much higher than the WHO Guide level for drinking water.
  • The water and seston MCYSTs concentrations, along with the existence of the two potentially toxic cyanobacterial phylotypes, raised two questions: a) whether Carassius gibelio individuals of the lake were affected and b) if yes, in what capacity? C. gibelio is a member of the family Cyprinidae. It is not a widely commercial fish, but is consumed in many regions of Greece. It is omnivorous; feeding on plankton, zoobenthos, invertebrates, plant material, and detritus (Specziár et al., 1997; 1998; Kottelat and Freyhof, 2007). However, as a result to its method of water filtration in order to obtain its main food source, large quantities of filamentous and colonial cyanobacteria often occur in its digestive tract (Kolmakov and Gladyshev, 2003). MCYSTs Ananiadis, C.I. 1959. Limnological study of Lake Karla. Bulletin de l’Institut Oc´eanographique, 1083: 1–19.
  • Bartram, J., Burch, M., Falconer, I.R., Jones, G. and Kuiper-Goodman, T. 1999. Situation assessment, planning and management. In: I. Chorus, J. Bartram (Eds), Toxic cyanobacteria in water, Taylor and Francis, London, New York: 179-209.
  • Carbis, C.R., Rawlin, G.T., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1996. The histopathology of carp, Cyprinus carpio L., exposed to microcystins by gavage, immersion and intraperitoneal administration. Journal of Fish Diseases, 19: 199–207. doi: 1111/j.1365-2761.1996.tb00126.x
  • Carbis, C.R., Rawlin, G.T., Grant, P., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1997. A study of feral carp, Cyprinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health. Journal of Fish Diseases, 20: 81–91. doi: 10.1046/j.1365-2761.1997.d01-111.x Carmichael, W.W., Azevedo, S.M.F.O., An, J.S., Molica, R.J., Jochimsen, E.M., Lau, S., Rinehart, K.L., Shaw, G.R. and Eaglesham, G.K. 2001. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environmental Health Perspectives, 109: 663-668. doi: 10.1289/ehp.01109663
  • Chatzinikolaou, Y., Ioannou, A. and Lazaridou, M. 2010. Intrabasin spatial approach on pollution load estimation in a large Mediterranean river. Desalination, 250: 118–129. doi: 1016/j.desal.2008.12.062.
  • Chorus, I. 2001. Cyanotoxin occurrence in freshwaters-a summary of survey results from different countries. In: I. Chorus (Ed.), Cyanotoxins: Occurrence, causes consequences, Spinger, Berlin: 75-78.
  • Codd, G.A. 1995. Cyanobacterial toxins: occurrence, properties and biological significance. Water Science and Technology, 32(4): 149-156. doi: 10.1016/02731223(95)00692-3.
  • Codd, G.A., Chorus, I and Burch, M. 1999. Design of monitoring programmes. In: I. Chorus, J. Bartram (Eds), Toxic Cyanobacteria in water: a guide to their public health consequences, monitoring and management, E & FN Spon, London: 313-328.
  • Cooley, H.M., Evans, R.E. and Klaverkamp, J.F. 2000. Toxicology of dietary uranium in lake whitefish (Coregonus clupeaformis). Aquatic Toxicology, 48: 495–515. doi: 10.1016/S0166-445X(99)00057-0.
  • Dietrich, D. and Hoeger, S. 2005. Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? Toxicology and Applied Pharmacology, 203: 273–289. doi: 1016/j.taap.2004.09.005.
  • Dos Santos, A.P.M.E. and Bracarense, A.P.F.R.L. 2008. Hepatotoxicity associated with microcystins. Semina:Ciencias Agrarias, 29: 4174 doi: 10.5433/1679-0359.2008v29n2p417
  • Ernst, B. 2008. Investigations of the impact of toxic cyanobacteria on fish. PhD thesis, Constance, Germany: Universität Konstanz. Dissertation, University of Kostanz.
  • Fisher, W., Dietrich, D. 2000a. Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicology and Applied Pharmacology, 164: 73– doi: 10.1006/taap.1999.8861.
  • Fischer, W. and Dietrich, D. 2000b. Toxicity of the cyanobacterial cyclic heptapeptide toxins microcystin LR and-RR in early life-stages of the African clawed frog (Xenopus laevis). Aquatic Toxicology, 49: 189– 1 doi: 10.1016/S0166-445X(99)00079-X.
  • Fournie, J. W., Courtney, L.A. 2002. Histopathological evidence of regeneration following hepatotoxic effects of the cyanotoxin Microcystin-LR in the hardhead catfish and Gulf killifish. Journal of Aquatic Animal Health, 14: 273doi: 1577/15488667(2002)014<0273:HEORFH>2.0.CO;2.
  • Hawkins, B.T. and Davis, T.P. 2005. The blood-brain barrier/neurovascular unit in health and disease. Pharmacological Reviews, 57: 173-85. doi: 1124/pr.57.2.4.
  • Huisman, J., Matthijs, H.C.P. and Visser, P.M. 2005. Harmful cyanobacteria. Springer, Berlin, 243 pp.
  • Kagalou, I., Kormas, K.A., Papadimitriou, T., Katsiapi, M., Genitsaris, S. and Moustaka-Gouni, M. 2012. Greece: occurrence, monitoring and risk management of cyanobacteria and cyanotoxins. In: I. Chorus (Ed), Current approaches to cyanotoxin risk assessment, risk management and regulations in different countries, Federal Environmental Agency (Umweltbundesamt), Berlin: 71-78.
  • Kagalou, I., Papadimitriou, T., Bacopoulos, V. and Leonardos, I. 2008. Assessment of microcystins in lake water and the omnivorous fish (Carassius gibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environmental Monitoring and Assessment, 137: 185-195. doi: 1007/s10661-007-9739-6.
  • Katsiapi, M., Moustaka-Gouni, M., Vardaka, E. and Kormas, K.A. 20 Different phytoplankton descriptors show asynchronous changes in a shallow urban lake (L. Kastoria, Greece) after sewage diversion. Fundamental and Applied Limnology, 182:219-230. doi: 10.1127/1863-9135/2013/0362
  • Kolmakov, V. and Gladyshev, M. 2003. Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crusian carp. Aquatic Ecology, 37: 237-2 doi: 1023/A:1025801326088.
  • Kormas, K.A., Gkelis, S., Vardaka, E., Moustaka-Gouni, M. 20 Morphologic and molecular analysis of bloomforming Cyanobacteria in two eutrophic, shallow Mediterranean lakes. Limnologica, 41: 167-173. doi: 1016/j.limno.2010.10.003.
  • Kotak, B.J., Semalulu, S., Friytz, D.L., Prepas, E.E., Hrudey, S.E., Coppock, R.W. 1996. Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). Toxicon, 34: 517–25. doi: 10.1016/00410101(96)00009-8.
  • Kottelat, M. and Freyhof, J. 2007. Handbook of European freshwater fishes. Publications Kottelat, Berlin, 646 pp.
  • Lang, T., Wosniok, W., Barsiene, J., Broeg, K., Kopecka, J. and Parkkonen, J. 2006. Liver histopathology in Baltic flounder (Platichthys flesus) as indicator of biological effects of contaminants. Marine Pollution Bulletin, 53: 488-4 doi: 1016/j.marpolbul.2005.11.008.
  • Li, L., Xie, P., Li, S., Qiu, T., Guo, L. 2007. Sequential ultrastructural and biochemical changes induced in vivo by the hepatotoxic microcystins in liver of the phytoplanktivorous silver carp Hypophthalmichthys molitrix. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146: 357–367. doi: 1016/j.cbpc.2007.04.008.
  • Malbrouck, C., Kestemont, P. 2006. Effects of Microcystins on fish. Environmental Toxicology and Chemistry, 25: 72–86. doi: 10.1897/05-029R.1.
  • Mitsoura, A., Kagalou, I., Papaioannou, N., Berillis, P., Mente, E. and Papadimitriou T. 2013. The presence of microcystins in fish Cyprinus carpio tissues: an histopathological study. International Aquatic Research, 5: 8. doi:10.1186/2008-6970-5-8
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There are 46 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Berillis Panagiotis This is me

Papadimitriou Theodoti This is me

Petridou Evi This is me

Kormas Konstantinos This is me

Kagalou Ifigenia This is me

Publication Date July 7, 2014
Published in Issue Year 2014 Volume: 14 Issue: 1

Cite

APA Panagiotis, B., Theodoti, P., Evi, P., Konstantinos, K., et al. (2014). Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria. Turkish Journal of Fisheries and Aquatic Sciences, 14(1). https://doi.org/10.4194/1303-2712-v14_1_23
AMA Panagiotis B, Theodoti P, Evi P, Konstantinos K, Ifigenia K. Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria. Turkish Journal of Fisheries and Aquatic Sciences. February 2014;14(1). doi:10.4194/1303-2712-v14_1_23
Chicago Panagiotis, Berillis, Papadimitriou Theodoti, Petridou Evi, Kormas Konstantinos, and Kagalou Ifigenia. “Brain and Liver Histopathological Examination of Carassius Gibelio from A Newly Reconstructed Lake With Toxic Cyanobacteria”. Turkish Journal of Fisheries and Aquatic Sciences 14, no. 1 (February 2014). https://doi.org/10.4194/1303-2712-v14_1_23.
EndNote Panagiotis B, Theodoti P, Evi P, Konstantinos K, Ifigenia K (February 1, 2014) Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria. Turkish Journal of Fisheries and Aquatic Sciences 14 1
IEEE B. Panagiotis, P. Theodoti, P. Evi, K. Konstantinos, and K. Ifigenia, “Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria”, Turkish Journal of Fisheries and Aquatic Sciences, vol. 14, no. 1, 2014, doi: 10.4194/1303-2712-v14_1_23.
ISNAD Panagiotis, Berillis et al. “Brain and Liver Histopathological Examination of Carassius Gibelio from A Newly Reconstructed Lake With Toxic Cyanobacteria”. Turkish Journal of Fisheries and Aquatic Sciences 14/1 (February 2014). https://doi.org/10.4194/1303-2712-v14_1_23.
JAMA Panagiotis B, Theodoti P, Evi P, Konstantinos K, Ifigenia K. Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria. Turkish Journal of Fisheries and Aquatic Sciences. 2014;14. doi:10.4194/1303-2712-v14_1_23.
MLA Panagiotis, Berillis et al. “Brain and Liver Histopathological Examination of Carassius Gibelio from A Newly Reconstructed Lake With Toxic Cyanobacteria”. Turkish Journal of Fisheries and Aquatic Sciences, vol. 14, no. 1, 2014, doi:10.4194/1303-2712-v14_1_23.
Vancouver Panagiotis B, Theodoti P, Evi P, Konstantinos K, Ifigenia K. Brain and Liver Histopathological Examination of Carassius gibelio from A Newly Reconstructed Lake with Toxic Cyanobacteria. Turkish Journal of Fisheries and Aquatic Sciences. 2014;14(1).