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Current IssueEditorial BoardOnline First ArticlesArchive

Research Article

volume 53 issue 6 (june 2019) : 751-755,   Doi: 10.18805/ijar.B-910

Pattern of renal pathology in fish from Al-Hassa waterways, Saudi Arabia
 

A
Ashraf Abdel-Moneim
O
Omar Elmenshawy
M
Mohamed Al-Kahtani
A
Abdalla Sayed
M
Manal Alfwuaires
1Department of Biology, Faculty of Science, King Faisal University, Al-Hassa, Saudi Arabia.
Cite article:- Abdel-Moneim Ashraf, Elmenshawy Omar, Al-Kahtani Mohamed, Sayed Abdalla, Alfwuaires Manal (2018). Pattern of renal pathology in fish from Al-Hassa waterways, Saudi Arabia. Indian Journal of Animal Research. 53(6): 751-755. doi: 10.18805/ijar.B-910.

ABSTRACT

Pollution of aquatic environment is a great concern worldwide. The teleostean kidney is one of the first organ to be affected by contaminants in water. The aim of this study is to assess histological changes of Oreochromis niloticus kidney collected from spring canals in Al-Hassa, Saudi Arabia. We report histological alterations in the kidney tissue of fish collected from three sites, namely Al-Jawhariya (site #1), Um-Sabah (site #2) and Al-Khadoud spring (site #3). The histopathological studies revealed relative differences in the severity of organ lesions among the three sites. The overall results showed that kidney architecture of fish samples was markedly disrupted. The major symptoms were dilation of the glomerular capillaries, reduction of Bowman’s space, degeneration of tubular epithelium, tubule cast deposition, and accumulation of pigmented macrophages (i.e., melanomacrophages). The histological damage in the kidney of O. niloticus is an evidence of the poor environmental quality of these spring canals. It appears that these wetland areas are still threatened by human activities and environmental degradation.

REFERENCES

  1. Abdel-Moneim, A.M., Abu El-Saad, A.M., Hussein, H.K., Dekinesh, S.I. (2012a). Gill oxidative stress and histopathological biomarkers of pollution impacts in Nile tilapia from Lake Mariut and Lake Edku, Egypt. Journal of Aquatic Animal Health, 24: 148–    160. DOI: 10.1080/08997659.2012.675924.
  2. Abdel-Moneim, A.M., Al-Kahtani, M.A., Elmenshawy, O.M. (2012b). Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere, 88: 1028–1035. DOI: 10.1016/    j.chemosphere.2012.04.001.
  3. Ahmed, Q., Benzer, S., Yousuf, F. (2016). Distribution of heavy metals in different tissues of Indian Mackerel from Karachi Fish Harbour, Karachi, Pakistan. Indian Journal of Animal Research, 50: 759–763. DOI: 10.18805/ijar.11423.
  4. Al-Kahtani, M.A. (2009). Accumulation of heavy metals in Tilapia Fish (Oreochromis niloticus) from Al-Khadoud Spring, Al-Hassa, Saudi Arabia. American Journal of Applied Sciences, 6: 2024–2029. DOI: 10.3844/ajassp.2009.2024.2029.
  5. Ayas, Z., Ekmekci, G., Ozmen, M.and Yerli, S. V. (2007). Histopathological changes in the livers and kidneys of fish in Sariyar Reservoir, Turkey. Environ. Environmental Toxicology and Pharmacology, 23: 242–249. DOI: 10.1016/j.etap.2006.11.003.
  6. Ben Ameur, W., and de Lapuente, J., El Megdiche, Y., Barhoumi, B., Trabelsi, S., Camps, L., Serret, J., Ramos-López, D., Gonzalez-    Linares, J., Driss, M.R., Borràs, M. (2012). Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Marine Pollution Bulletin, 64: 241–251. DOI: 10.1016/j.marpolbul.2011.11.026.
  7. Bernet, D., Schmidt, H., Meier, W., Burkhardt-Holm, P., and Wahli, T. (1999). Histopathology in fish: Proposal for a protocol to assess aquatic pollution. Journal of Fish Diseases, 22: 25–34. DOI: 10.1046/j.1365-2761.1999.00134.x.
  8. Camargo, M.M.P., and Martinez, C.B.R. (2007). Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropical Ichthyology, 5: 327–336. DOI: 10.1590/S1679-62252007000300013.
  9. Corsi, I., Mariottini, M., Sensini, C., Lancini, L., and Focardi, S. (2003). Fish as Bioindicators of Brackish Ecosystem Health: Integrating Biomarker Responses and Target Pollutant Concentrations. Oceanologica Acta, 26: 129-38. DOI: 10.1016/S0399-    1784(02)01237-9.
  10. Costa, P.M., Diniz, M.S., Caeiro, S., Lobo, J., Martins, M., Ferreira, A.M., Caetano, M., et al. (2009). Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: A weighted indices approach. Aquatic Toxicology, 92: 202–212. DOI: 10.1016/j.aquatox.2008.12.009.
  11. Costa, P.M., Caeiro, S., Lobo, J., Martins, M., Ferreira, A.M., Caetano, M., Vale, C., et al. (2011). Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish. Marine Pollution Bulletin, 62: 55–65. DOI: 10.1016/    j.marpolbul.2010.09.009.
  12. Fernandes, C., Fontaínhas-Fernandes, A., Rocha, E., Salgado, M.A. (2008). Monitoring pollution in Esmoriz-Paramos lagoon, Portugal: Liver histological and biochemical effects in Liza saliens. Environmental Monitoring and Assessment, 145: 315–322. DOI: 10.1007/s10661-007-0041-4.
  13. Gernhöfer, M., Pawert, M., Schramm, M., Müller, E., Triebskorn, R. (2001). Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams. Journal of Aquatic Ecosystem Stress and Recovery, 8: 241–260. DOI: 10.1023/    A:1012958804442.
  14. Ghedira, J., Jebali, J., Bouraoui, Z., Banni, M., Guerbej, H., Boussetta, H. (2010). Metallothionein and metal levels in liver, gills and kidney of Sparus aurata exposed to sublethal doses of cadmium and copper. Fish Physiology and Biochemistry, 36: 101–    107. DOI: 10.1007/s10695-008-9295-1.
  15. Hinton, D.E., and Lauren, D.J. (1990). Integrative histopathological approaches to detecting effects of environmental stressors on fishes. American Fisheries Society Symposium, pp. 51-66. 
  16. Kirubagaran, R., and Joy, K.P. (1988). Toxic effects of three mercurial compounds on survival, and histology of the kidney of the catfish Clarias batrachus (L.). Ecotoxicology and Environmental Safety, 15: 171–179. DOI: 10.1016/0147-6513(88)90069-3.
  17. Lukin, A., Sharova, J., Belicheva, L., and Camus, L. (2011). Assessment of fish health status in the Pechora River: Effects of contamination. Ecotoxicology and Environmental Safety, 74(3): 355–365. DOI: 10.1016/j.ecoenv.2010.10.022.
  18. Meinelt, T., Krüger, R., Pietrock, M., Osten, R., Steinberg, C. (1997). Mercury pollution and macrophage centres in pike (Esox lucius) tissues. Environmental Science and Pollution Research International, 4: 32–36. DOI: 10.1007/BF02986262.
  19. Meyers, T. R., and Hendricks J.D. (1985). Histopathology. Hemisphere Publishing Corporation, Washington, USA, pp. 283– 331.
  20. Obasohan, E.E., and Oronsaye, J.A.O. (2008). An investigation of the impact of municipal waste waters on the Diversity and Abundance of the Cichlid Fishes of Ogba River in Benin City, Nigeria. Indian Journal of Animal Research, 42: 1-9. 
  21. Oliva, M., Vicente-Martorell, J.J., Galindo-Riaño, M.D., Perales, J.A. (2013). Histopathological alterations in Senegal sole, Solea Senegalensis, from a polluted Huelva estuary (SW, Spain). Fish Physiology and Biochemistry, 39: 523–545. DOI: 10.1007/    s10695-012-9717-y.
  22. Oliveira Ribeiro, C.A., Vollaire, Y., Sanchez-Chardi, A., and Roche, H. (2005). Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquatic Toxicology, 74: 53–69. DOI: 10.1016/j.aquatox.2005.04.008.
  23. Ortiz, J.B., Canales, M.L.G.D.E., and Sarasquete, C. (2003). Histopathological changes induced by lindane (ã-HCH) in various organs of fishes. Ciencias Marinas, 67: 53–61. DOI: 10.3989/scimar.2003.67n153.
  24. Pritchard, J.B., and Bend, J.R. (1984). Mechanisms controlling the renal excretion of xenobiotics in fish: effects of chemical structure. Drug Metabolism Reviews, 15: 655-671. DOI: 10.3109/03602538409041075.
  25. Rand, G.M. (1996). Fundamentals of Aquatic Toxicology: Effects, Environmental Fate, and Risk Assessment. International Journal of Toxicology, 15: 453–54.
  26. Samanta, P., Bandyopadhyay, N., Pal, S., Mukherjee, A.K., Ghosh, A.R. (2015). Histopathological and ultramicroscopical changes in gill, liver and kidney of Anabas testudineus (Bloch) after chronic intoxication of almix (metsulfuron methyl 10.1%+chlorimuron ethyl 10.1%) herbicide. Ecotoxicology and Environmental Safety, 122: 360–367. DOI: 10.1016/j.ecoenv.2015.08.022.
  27. Samanta, P., Mukherjee, A.K., Pal, S., Kole, D., Ghosh, A.R. (2016). Toxic effects of glyphosate-based herbicide, Excel Mera 71 on gill, liver, and kidney of Heteropneustes fossilis under laboratory and field conditions. Journal of Microscopy and Ultrastructure, 4: 147–155. DOI: 10.1016/j.jmau.2016.01.002.
  28. Schwaiger, J., Wanke, R., Adam, S., Pawert, M., Hönnen, W., Triebskorn, R. (1997). The use of histopathological indicators to evaluate contaminant-related stress in fish. Journal of Aquatic Ecosystem Stress and Recovery, 6: 75–86. DOI: 10.1023/    A:1008212000208.
  29. Silva, A.G., Martinez, C.B.R. (2007). Morphological changes in the kidney of a fish living in an urban stream. Environmental Toxicology and Pharmacology, 23: 185–192. DOI:10.1016/j.etap.2006.08.009.
  30. Stentiford, G.D., Longshaw, M., Lyons, B.P., Jones, G., Green, M., Feist, S.W. (2003). Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Marine Environmental Research, 55: 137–159. DOI: 10.1016/    S0141-1136(02)00212-X.
  31. Takashima, F., Hibya T. (1995). An atlas of fish histology: normal and pathological features, 2nd edition, Tokyo, Kodansha.
  32. Teh, S.J., Adams, S.M., Hinton, D.E. (1997). Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquatic Toxicology, 37: 51–70. DOI: 10.1016/S0166-445X(96)00808-9.
  33. Thophon, S., Kruatrachue, M., Upatham, E.S., Pokethitiyook, P., Sahaphong, S., Jaritkhuan, S. (2003). Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environmental Pollution, 121: 307–320. DOI: 10.1016/S0269-7491(02)00270-1.
  34. Van der Oost, R., Beyer, J., and Vermeulen, N.P.E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology, 13: 57–149. DOI: 10.1016/S1382-6689(02)00126-6.
  35. Van Dyk, J.C., Cochrane, M.J., and Wagenaar, G.M. (2012). Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere, 87: 301–311. DOI: 10.1016/j.chemosphere.2011.12.002.
  36. Yasser, A.G., Naser, M.D. (2011). Impact of pollutants on fish collected from different parts of Shatt Al-Arab River: A histopathological study. Environmental Monitoring and Assessment, 181: 175–182. DOI: 10.1007/s10661-010-1822-8. 
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Indian Journal of Animal Research
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    Research Article

    volume 53 issue 6 (june 2019) : 751-755,   Doi: 10.18805/ijar.B-910

    Pattern of renal pathology in fish from Al-Hassa waterways, Saudi Arabia
     

    A
    Ashraf Abdel-Moneim
    O
    Omar Elmenshawy
    M
    Mohamed Al-Kahtani
    A
    Abdalla Sayed
    M
    Manal Alfwuaires
    1Department of Biology, Faculty of Science, King Faisal University, Al-Hassa, Saudi Arabia.
    Cite article:- Abdel-Moneim Ashraf, Elmenshawy Omar, Al-Kahtani Mohamed, Sayed Abdalla, Alfwuaires Manal (2018). Pattern of renal pathology in fish from Al-Hassa waterways, Saudi Arabia. Indian Journal of Animal Research. 53(6): 751-755. doi: 10.18805/ijar.B-910.

    ABSTRACT

    Pollution of aquatic environment is a great concern worldwide. The teleostean kidney is one of the first organ to be affected by contaminants in water. The aim of this study is to assess histological changes of Oreochromis niloticus kidney collected from spring canals in Al-Hassa, Saudi Arabia. We report histological alterations in the kidney tissue of fish collected from three sites, namely Al-Jawhariya (site #1), Um-Sabah (site #2) and Al-Khadoud spring (site #3). The histopathological studies revealed relative differences in the severity of organ lesions among the three sites. The overall results showed that kidney architecture of fish samples was markedly disrupted. The major symptoms were dilation of the glomerular capillaries, reduction of Bowman’s space, degeneration of tubular epithelium, tubule cast deposition, and accumulation of pigmented macrophages (i.e., melanomacrophages). The histological damage in the kidney of O. niloticus is an evidence of the poor environmental quality of these spring canals. It appears that these wetland areas are still threatened by human activities and environmental degradation.

    REFERENCES

    1. Abdel-Moneim, A.M., Abu El-Saad, A.M., Hussein, H.K., Dekinesh, S.I. (2012a). Gill oxidative stress and histopathological biomarkers of pollution impacts in Nile tilapia from Lake Mariut and Lake Edku, Egypt. Journal of Aquatic Animal Health, 24: 148–    160. DOI: 10.1080/08997659.2012.675924.
    2. Abdel-Moneim, A.M., Al-Kahtani, M.A., Elmenshawy, O.M. (2012b). Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere, 88: 1028–1035. DOI: 10.1016/    j.chemosphere.2012.04.001.
    3. Ahmed, Q., Benzer, S., Yousuf, F. (2016). Distribution of heavy metals in different tissues of Indian Mackerel from Karachi Fish Harbour, Karachi, Pakistan. Indian Journal of Animal Research, 50: 759–763. DOI: 10.18805/ijar.11423.
    4. Al-Kahtani, M.A. (2009). Accumulation of heavy metals in Tilapia Fish (Oreochromis niloticus) from Al-Khadoud Spring, Al-Hassa, Saudi Arabia. American Journal of Applied Sciences, 6: 2024–2029. DOI: 10.3844/ajassp.2009.2024.2029.
    5. Ayas, Z., Ekmekci, G., Ozmen, M.and Yerli, S. V. (2007). Histopathological changes in the livers and kidneys of fish in Sariyar Reservoir, Turkey. Environ. Environmental Toxicology and Pharmacology, 23: 242–249. DOI: 10.1016/j.etap.2006.11.003.
    6. Ben Ameur, W., and de Lapuente, J., El Megdiche, Y., Barhoumi, B., Trabelsi, S., Camps, L., Serret, J., Ramos-López, D., Gonzalez-    Linares, J., Driss, M.R., Borràs, M. (2012). Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Marine Pollution Bulletin, 64: 241–251. DOI: 10.1016/j.marpolbul.2011.11.026.
    7. Bernet, D., Schmidt, H., Meier, W., Burkhardt-Holm, P., and Wahli, T. (1999). Histopathology in fish: Proposal for a protocol to assess aquatic pollution. Journal of Fish Diseases, 22: 25–34. DOI: 10.1046/j.1365-2761.1999.00134.x.
    8. Camargo, M.M.P., and Martinez, C.B.R. (2007). Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropical Ichthyology, 5: 327–336. DOI: 10.1590/S1679-62252007000300013.
    9. Corsi, I., Mariottini, M., Sensini, C., Lancini, L., and Focardi, S. (2003). Fish as Bioindicators of Brackish Ecosystem Health: Integrating Biomarker Responses and Target Pollutant Concentrations. Oceanologica Acta, 26: 129-38. DOI: 10.1016/S0399-    1784(02)01237-9.
    10. Costa, P.M., Diniz, M.S., Caeiro, S., Lobo, J., Martins, M., Ferreira, A.M., Caetano, M., et al. (2009). Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: A weighted indices approach. Aquatic Toxicology, 92: 202–212. DOI: 10.1016/j.aquatox.2008.12.009.
    11. Costa, P.M., Caeiro, S., Lobo, J., Martins, M., Ferreira, A.M., Caetano, M., Vale, C., et al. (2011). Estuarine ecological risk based on hepatic histopathological indices from laboratory and in situ tested fish. Marine Pollution Bulletin, 62: 55–65. DOI: 10.1016/    j.marpolbul.2010.09.009.
    12. Fernandes, C., Fontaínhas-Fernandes, A., Rocha, E., Salgado, M.A. (2008). Monitoring pollution in Esmoriz-Paramos lagoon, Portugal: Liver histological and biochemical effects in Liza saliens. Environmental Monitoring and Assessment, 145: 315–322. DOI: 10.1007/s10661-007-0041-4.
    13. Gernhöfer, M., Pawert, M., Schramm, M., Müller, E., Triebskorn, R. (2001). Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams. Journal of Aquatic Ecosystem Stress and Recovery, 8: 241–260. DOI: 10.1023/    A:1012958804442.
    14. Ghedira, J., Jebali, J., Bouraoui, Z., Banni, M., Guerbej, H., Boussetta, H. (2010). Metallothionein and metal levels in liver, gills and kidney of Sparus aurata exposed to sublethal doses of cadmium and copper. Fish Physiology and Biochemistry, 36: 101–    107. DOI: 10.1007/s10695-008-9295-1.
    15. Hinton, D.E., and Lauren, D.J. (1990). Integrative histopathological approaches to detecting effects of environmental stressors on fishes. American Fisheries Society Symposium, pp. 51-66. 
    16. Kirubagaran, R., and Joy, K.P. (1988). Toxic effects of three mercurial compounds on survival, and histology of the kidney of the catfish Clarias batrachus (L.). Ecotoxicology and Environmental Safety, 15: 171–179. DOI: 10.1016/0147-6513(88)90069-3.
    17. Lukin, A., Sharova, J., Belicheva, L., and Camus, L. (2011). Assessment of fish health status in the Pechora River: Effects of contamination. Ecotoxicology and Environmental Safety, 74(3): 355–365. DOI: 10.1016/j.ecoenv.2010.10.022.
    18. Meinelt, T., Krüger, R., Pietrock, M., Osten, R., Steinberg, C. (1997). Mercury pollution and macrophage centres in pike (Esox lucius) tissues. Environmental Science and Pollution Research International, 4: 32–36. DOI: 10.1007/BF02986262.
    19. Meyers, T. R., and Hendricks J.D. (1985). Histopathology. Hemisphere Publishing Corporation, Washington, USA, pp. 283– 331.
    20. Obasohan, E.E., and Oronsaye, J.A.O. (2008). An investigation of the impact of municipal waste waters on the Diversity and Abundance of the Cichlid Fishes of Ogba River in Benin City, Nigeria. Indian Journal of Animal Research, 42: 1-9. 
    21. Oliva, M., Vicente-Martorell, J.J., Galindo-Riaño, M.D., Perales, J.A. (2013). Histopathological alterations in Senegal sole, Solea Senegalensis, from a polluted Huelva estuary (SW, Spain). Fish Physiology and Biochemistry, 39: 523–545. DOI: 10.1007/    s10695-012-9717-y.
    22. Oliveira Ribeiro, C.A., Vollaire, Y., Sanchez-Chardi, A., and Roche, H. (2005). Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquatic Toxicology, 74: 53–69. DOI: 10.1016/j.aquatox.2005.04.008.
    23. Ortiz, J.B., Canales, M.L.G.D.E., and Sarasquete, C. (2003). Histopathological changes induced by lindane (ã-HCH) in various organs of fishes. Ciencias Marinas, 67: 53–61. DOI: 10.3989/scimar.2003.67n153.
    24. Pritchard, J.B., and Bend, J.R. (1984). Mechanisms controlling the renal excretion of xenobiotics in fish: effects of chemical structure. Drug Metabolism Reviews, 15: 655-671. DOI: 10.3109/03602538409041075.
    25. Rand, G.M. (1996). Fundamentals of Aquatic Toxicology: Effects, Environmental Fate, and Risk Assessment. International Journal of Toxicology, 15: 453–54.
    26. Samanta, P., Bandyopadhyay, N., Pal, S., Mukherjee, A.K., Ghosh, A.R. (2015). Histopathological and ultramicroscopical changes in gill, liver and kidney of Anabas testudineus (Bloch) after chronic intoxication of almix (metsulfuron methyl 10.1%+chlorimuron ethyl 10.1%) herbicide. Ecotoxicology and Environmental Safety, 122: 360–367. DOI: 10.1016/j.ecoenv.2015.08.022.
    27. Samanta, P., Mukherjee, A.K., Pal, S., Kole, D., Ghosh, A.R. (2016). Toxic effects of glyphosate-based herbicide, Excel Mera 71 on gill, liver, and kidney of Heteropneustes fossilis under laboratory and field conditions. Journal of Microscopy and Ultrastructure, 4: 147–155. DOI: 10.1016/j.jmau.2016.01.002.
    28. Schwaiger, J., Wanke, R., Adam, S., Pawert, M., Hönnen, W., Triebskorn, R. (1997). The use of histopathological indicators to evaluate contaminant-related stress in fish. Journal of Aquatic Ecosystem Stress and Recovery, 6: 75–86. DOI: 10.1023/    A:1008212000208.
    29. Silva, A.G., Martinez, C.B.R. (2007). Morphological changes in the kidney of a fish living in an urban stream. Environmental Toxicology and Pharmacology, 23: 185–192. DOI:10.1016/j.etap.2006.08.009.
    30. Stentiford, G.D., Longshaw, M., Lyons, B.P., Jones, G., Green, M., Feist, S.W. (2003). Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Marine Environmental Research, 55: 137–159. DOI: 10.1016/    S0141-1136(02)00212-X.
    31. Takashima, F., Hibya T. (1995). An atlas of fish histology: normal and pathological features, 2nd edition, Tokyo, Kodansha.
    32. Teh, S.J., Adams, S.M., Hinton, D.E. (1997). Histopathologic biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquatic Toxicology, 37: 51–70. DOI: 10.1016/S0166-445X(96)00808-9.
    33. Thophon, S., Kruatrachue, M., Upatham, E.S., Pokethitiyook, P., Sahaphong, S., Jaritkhuan, S. (2003). Histopathological alterations of white seabass, Lates calcarifer, in acute and subchronic cadmium exposure. Environmental Pollution, 121: 307–320. DOI: 10.1016/S0269-7491(02)00270-1.
    34. Van der Oost, R., Beyer, J., and Vermeulen, N.P.E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology, 13: 57–149. DOI: 10.1016/S1382-6689(02)00126-6.
    35. Van Dyk, J.C., Cochrane, M.J., and Wagenaar, G.M. (2012). Liver histopathology of the sharptooth catfish Clarias gariepinus as a biomarker of aquatic pollution. Chemosphere, 87: 301–311. DOI: 10.1016/j.chemosphere.2011.12.002.
    36. Yasser, A.G., Naser, M.D. (2011). Impact of pollutants on fish collected from different parts of Shatt Al-Arab River: A histopathological study. Environmental Monitoring and Assessment, 181: 175–182. DOI: 10.1007/s10661-010-1822-8. 
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