Main Article Content
Abstract
The cultured and wild specimens of the Nile tilapia (Oreochromis niloticus) are often infected by different hazardous as helminths; protozoa and arthropod which cause various degrees of diseases in such fish. The aim of this study was to record the most common protozoan parasites in the Nile tilapia in Egypt, and also assessment of the immunological changes through analyzing two genes (Tumor Necrosis Factor alpha, TNF-α; and Interlukin-1β, IL- 1β) in the infected fishes using qRT-PCR. Therefore, each fish individual was examined carefully, and smears were prepared from each organ; stained with Giemsa dye and examined under a light microscope. qRT-PCR was performed on infected tissues (skin and gills) by various collected parasites. Four trichodinid species (Trichodinella heterodentata, T. centrostrigeata, T. epizootica, Paratrichodina Africana,) were isolated and identified; also two Myxobolus spp. (M. tilapiae and M. heterosporous) were fully described. In skin, TNF-α in M. tilapiae and mixed groups were nearly similar and were significantly higher than Trichodina spp. group. IL-1β of M. tilapiae group was significantly lower than that of the mixed group; Trichodina spp. and control groups. In gills, TNF-α of the mixed group showed the significantly highest value. IL-1β was nearly same in all groups. We conclude that the skin is nearly higher in upregulation of the two studied genes comparing to the gills analysis, since it is considered as the first barrier in fish and contains many immunological defined cells.
Keywords
Nile tilapia
Tumor Necrosis Factor alpha
Interlukin-1β
Real-time Polymerase Chain Reaction.
Article Details
License
The authors transfer the copyrights of their papers to the Iranian Society of Ichthyology. However, the information could be used in accordance with the Creative Commons licence (Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
How to Cite
YOUNIS, N. A., Attia, M. M., & SALEH, N. M. (2021). Analysis of TNF alpha and Interlukin-1β genes in Oreochromis niloticus: inflammatory responses induced by Myxobolus spp. and Trichodina spp. Iranian Journal of Ichthyology, 8(1), 30–40. https://doi.org/10.22034/iji.v8i1.450
References
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Abdel-Ghaffar, F.; Abdel-Gaber, R.; Maher, S.; El Deeb, N.; Kamel, R.; Al Quraishy. S. & Mehlhorn, H. 2016. Morphological and ultrastructural characteristics of Myxobolus ridibundae n. sp. (Myxosporea: Bivalvulida) infecting the testicular tissue of the marsh frog Ranaridibunda (Amphibia: Ranidae) in Egypt. Parasitology Research 116: 133-141.
Abdel-Azeem, S.A.; Heba, M.A.; Thabet, S.; Eman, Z.; Khalid, E.I. & Al-Quraishy, S. 2015. Two Myxobolus spp. infecting the kidney of Nile tilapia (Oreochromis niloticus) in the River Nile at Beni-Suef governorate, Egypt, and the associated renal changes. Parasitology Research 114: 1107-1112.
Abbas, A.Y.; Abd El-tawab, F.G. & Ebtsam, A.A.T. 2009. Studies on some prevailing parasites affecting Oreochromis niloticus fingerlings with atrial of treatment. Egypt Journal of Aquatic Biology and Fish 13: 135-148.
Akbari, M. & Taghizadeh, V.; Heidarieh, M. & Hajimoradloo, A. 2017. The key role of Tumor Necrosis Factor alpha (TNF-α) in vaccinated rainbow trout via irradiated Ichthyophthirius multifiliis trophont. Veterinary Archive 87: 229-237.
Al-Rasheid, K.A.; Ali, M.A.; Sakran, T.; Baki, A.A.A. & Ghaffar, F.A.A. 2000. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some River Nile fish, Egypt. Parasitology International, 49(2): 131-137.
Attia, M.M.; El-Gameel, S.M. & Ismael, E. 2020. Evaluation of tumor necrosis factor-alpha (TNF-α); gamma interferon (IFN-γ) genes and oxidative stress in sheep: immunological responses induced by Oestrus ovis (Diptera: Oestridae) infestation. Journal of Parasitic Disease 44: 332-337.
Basson, L. & Van As, J.G. 1994. Trichodinid (Ciliophora: Peritrichia) from a calanoid copepod and catfish from South Africa and notes on host specificity. Systematic Parasitology 18: 147-158.
Ben-David, J.; Atkinson, S.D.; Pollak, Y.; Yossifon, G.; Shavit, U.; Bartholomew, J.L.; Lotan, T. 2016. Myxozoan polar tubules display structural and functional variation. Parasite and Vectors 9: 1-6.
Carriero, M.M.; Adriano, E.A.; Silva, M.R.M.; Ceccarelli, P.A. & Maia, A.A.M. 2013. Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLOS One 8: e73713.
Dickerson, H.W. 2012. Ichthyophthirius multifiliis. In: Patrick, K.B. & Woo, T.K. (eds.), Fish Parasites: Pathobiology and Protection. CABI, Wallingford. Pp: 55-72.
Eissa, A.E.; Said, K.A.; Younis, N.A.; Dessouki, A.A.; Maather, M.E.M.M.; Abu Mhara, A.A. & Abdelsalam, M. 2020. Myxobolus episquamalis infection in farmed flathead grey mullet Mugil cephalus L. and thin-lipped mullet Liza ramada. Aquaculture International 28: 363-376.
Fall, M.; Fomena, A.; Kostoingué, B.; Diebakate, C.; Faye, N. & Toguebaye, B.S. 2000. Myxosporidies (Myxozoa, Myxosporea) parasites des poissons Cichlidae du Cameroun, du Sénégal et du Tchad avec la description de deux nouvelles espéces. Annales des Sciences Naturelles-Zoologie et Biologie 21: 81-92.
Feist, S.W. & Longshaw, M. 2006. Phylum myxozoa. In: Woo, P.T.K. (ed.), Fish Diseases and Disorders. Protozoan and Metazoan Infections. CAB International, Oxfordshire. pp: 230-296.
Fomena, A. & Bouix, G. 1997. Myxosporea (Protozoa: Myxozoa) of freshwater fishes in Africa: keys to genera and species. Systematic Parasitology 37: 161-178.
Gómez, D.; Bartholomew, J. & Sunyer, J.O. 2014. Biology and mucosal immunity to Myxozoans. Developmental and Comparative Immunology 43: 243-256.
Gonzalez, S.F.; Buchmann, K. & Nielsen, M.E. 2007. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: Inflammatory responses caused by the ectoparasite Ichthyophthirius multifiliis. Fish & Shellfish Immunology 22: 641-650.
Heinecke, R.D. & Buchmann, K. 2013. Inflammatory response of Rainbow trout Oncorhynchus mykiss (Walbaum, 1792) larvae against Ichthyophthirius multifiliis. Fish & Shellfish Immunology 34: 521-528.
Hutson, J.C. 1993. Secretion of tumor necrosis factor alpha by testicular macrophages. Journal of Reproductive Immunology 23: 63-72.
Kaur, H. & Gupta, A. 2015. Genetic relatedness provides support for a species complex of myxosporeans infecting the Indian major carp, Labeo rohita. Animal Biology 65: 337-347.
Khaled, A.S.A.; Mohammed, A.A.; Thabit, S.; Abdel Azeem, A. & Fathy A.A. 2000. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some River Nile fish, Egypt. Parasitology International 49: 131-137.
Lindenstrøm, T.; Buchmann, K & Secombes, C.J. 2003. Gyrodactylus derjavini infection elicits IL-1ß expression in rainbow trout skin. Fish & Shellfish Immunology 15: 107-115.
Martinus, M.L.; Marchiori, N.; Noumbedakis, K. & Lami, F. 2012. Trichodina nobilis Chen, 1963 and Trichodina reticulate Hirschmann et partsch, 1955 from ornamental freshwater fishes in Brazil. Brazilian Journal of Biology 72: 281-286.
Mohammed, N.I.; Rabie, S.A.; Hussein, A.N.A. & Husssein, N.M. 2012. Infestation of Oreochromis niloticus and Tilapia zilli fresh-water fishes with myxosporean parasites, Qena province, Egypt. Egypt. Academic Journal of Biological Science 4: 235-246.
Mandira, S. & Bandyopadhyay, P.K. 2017. Seasonal incidence of protozoan parasitic infestation in ornamental fishes of West Bengal, India. Journal of Parasitic Disease 41: 523-526.
Ozer, A. & Erdem, O. 1998. Ectoparasitic protozoa fauna of the common carp (Cyprinus carpio L., 1758) caught in the Sinop region of Turkey. Journal of Natural History 32: 441-454.
Ozer, A. & Erdem, O. 1999. The relationship between occurrence of ectoparasites, temperature and culture conditions: A comparison of farmed and wild common carp (Cyprinus carpio L. 1758) in the Sinop region of northern Turkey. Journal of Natural History 33: 483-491.
Ozer, A. 2000. The occurrence of three species of Trichodina (Ciliophora: Peritrichia) on Cyprinus carpio in relation to culture conditions, seasonality and host characteristics. Acta Protozologica 39: 61-66.
Ozer, A. 2003. The occurrence of Trichodina domerguei Wallengren, 1897 and Trichodina tenuidens Faure-Fremiet, 1944 on three spined stickleback, Gasterosteus aculeatus L, 1758 found in a brackish and freshwater environment. Acta Protozologica 42: 41-46.
Ozer, A. 2003. Trichodina domerguei Wallengren, 1897 (Ciliophora: Peritrichia) Infestations on the Round Goby, Neogobius melanostomus Pallas, 1811 in relation to seasonality and host factors. Comparative Parasitology 70: 132-135.
Ovington, K.S.; Alleva, L.M.; & Kerr E.A. 1995. Cytokines and immunological control of Eimeria spp. International Journal of Parasitology 25: 1331-1351.
Ovington, K.S. & Smith N.C. 1992. Cytokines, free radicals and resistance to Eimeria. Parasitology Today 8: 422-426.
Picard-Sanchez, A.; Itziar, E.; Raquel, D.P.M.; Carla, P.; Oswaldo, P. & Ariadna, S.B. 2019. Acquired protective immune response in a fish-myxozoan model encompasses specific antibodies and inflammation resolution. Fish & Shellfish Immunology 90: 349-362.
Praveen, K.; Evans, D.L. & Jaso-Friedmann, L. 2006. Constitutive expression of tumor necrosis factor-alpha in cytotoxic cells of teleosts and its role in regulation of cell-mediated cytotoxicity. Molecular Immunology 43: 279-291.
Saha, M. & Bandyopadhyay, P.K. 2017. Parasitological and histological analysis of a new species of the genus Thalohanellus and description of a myxozoan parasite (Myxosporea: Bivalvulida) from cultured ornamental goldfish, Carassius auratus L. Aquaculture Reports 8: 8-15.
Simon, R.M.J. 2001. The occurrence and mechanisms of innate immunity against parasites in fish. Developmental and Comparative Immunology 25: 841-852.
Sigh, J.; Lindenstrom, T. & Buchmann, K. 2004a. Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophthirius multifiliis. Fish & Shellfish Immunology 7: 76-86.
Sigh, J.; Lindenstrom, T. & Bbuchmann, K. 2004b. The parasitic ciliate Ichthyophthirius multifliis induces expression of immune relevant genes in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 27: 409-417.
Smyth, J.D. 1994. Introduction to Animal Parasitology, 3rd Edition. Cambridge University Press, Cambridge.
Tantry, T.A.; Nazir, R.; Chishti, M.Z.; Ahmad, F.; Dar, G.H. & Dar, J.S. 2016. A report on the incidence of Trichodina heterodentata from fishes of Jammu, J & K, India. Journal of Parasitic Disease 40: 524-527.
Valladao, G.M.R.; Padua, S.B.; Gallani, S.U.; Menezes-filho, R.N.; Dias Neto, J.; Martins, M.L.; Ishikawa, M.M. & Pilarski, F. 2013. Paratrichodina africana (Ciliophora): A pathogenic gill parasite in farmed Nile tilapia. Veterinary Parasitology 197: 705-710.
Valladao, G.M.R.; Alves, L.O. & Pilarski, F. 2016. Trichodiniasis in Nile tilapia hatcheries: Diagnosis, Parasite: host-stage relationship and treatment. Aquaculture 451: 444-450.
Van As, J.G. & Basson, L. 1992. Trichodinid ectoparasites (Ciliophora: Peritrichida) of freshwater fishes of the Zambesi River System, with a reappraisal of host specificity. Systematic Parasitology 22: 81-109.
Wanderson, P.M.F.; Ligia, N.R.; Marcia Dias, R.D.; Renata Marinho, G.B.; Daniel, M. & Marcos, T.D. 2012. Protozoan and metazoan parasites of Nile tilapia oreochromis niloticus cultured in Brazil. Revista MVZ Córdoba 17: 2812-2819.
Wang, Q.; Yongyao, Y.; Xiaoting & Zhen X. 2019 Immune responses of fish to Ichthyophthirius multifiliis (Ich): A model for understanding immunity against protozoan parasites. Developmental and Comparative Immunology 93: 93-102.
Younis, N.A.; Laban, S.E.; Al-Mokaddem, A.K. & Attia, M.M. (2020) Immunological status and histopathological appraisal of farmed Oreochromis niloticus exposed to parasitic infections and heavy metal toxicity. Aquaculture International 28: 1-16.
Zhu, L.; Li, N.; Guan Z.; Li-xin, X. & Jian-zhong, S. 2013. Advances in research of fish immune-relevant genes: A comparative overview of innate and adaptive immunity in teleosts. Developmental and Comparative Immunology 39: 39-62.
References
Abdel-Ghaffar, F.; Abdel-Gaber, R.; Maher, S.; El Deeb, N.; Kamel, R.; Al Quraishy. S. & Mehlhorn, H. 2016. Morphological and ultrastructural characteristics of Myxobolus ridibundae n. sp. (Myxosporea: Bivalvulida) infecting the testicular tissue of the marsh frog Ranaridibunda (Amphibia: Ranidae) in Egypt. Parasitology Research 116: 133-141.
Abdel-Azeem, S.A.; Heba, M.A.; Thabet, S.; Eman, Z.; Khalid, E.I. & Al-Quraishy, S. 2015. Two Myxobolus spp. infecting the kidney of Nile tilapia (Oreochromis niloticus) in the River Nile at Beni-Suef governorate, Egypt, and the associated renal changes. Parasitology Research 114: 1107-1112.
Abbas, A.Y.; Abd El-tawab, F.G. & Ebtsam, A.A.T. 2009. Studies on some prevailing parasites affecting Oreochromis niloticus fingerlings with atrial of treatment. Egypt Journal of Aquatic Biology and Fish 13: 135-148.
Akbari, M. & Taghizadeh, V.; Heidarieh, M. & Hajimoradloo, A. 2017. The key role of Tumor Necrosis Factor alpha (TNF-α) in vaccinated rainbow trout via irradiated Ichthyophthirius multifiliis trophont. Veterinary Archive 87: 229-237.
Al-Rasheid, K.A.; Ali, M.A.; Sakran, T.; Baki, A.A.A. & Ghaffar, F.A.A. 2000. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some River Nile fish, Egypt. Parasitology International, 49(2): 131-137.
Attia, M.M.; El-Gameel, S.M. & Ismael, E. 2020. Evaluation of tumor necrosis factor-alpha (TNF-α); gamma interferon (IFN-γ) genes and oxidative stress in sheep: immunological responses induced by Oestrus ovis (Diptera: Oestridae) infestation. Journal of Parasitic Disease 44: 332-337.
Basson, L. & Van As, J.G. 1994. Trichodinid (Ciliophora: Peritrichia) from a calanoid copepod and catfish from South Africa and notes on host specificity. Systematic Parasitology 18: 147-158.
Ben-David, J.; Atkinson, S.D.; Pollak, Y.; Yossifon, G.; Shavit, U.; Bartholomew, J.L.; Lotan, T. 2016. Myxozoan polar tubules display structural and functional variation. Parasite and Vectors 9: 1-6.
Carriero, M.M.; Adriano, E.A.; Silva, M.R.M.; Ceccarelli, P.A. & Maia, A.A.M. 2013. Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLOS One 8: e73713.
Dickerson, H.W. 2012. Ichthyophthirius multifiliis. In: Patrick, K.B. & Woo, T.K. (eds.), Fish Parasites: Pathobiology and Protection. CABI, Wallingford. Pp: 55-72.
Eissa, A.E.; Said, K.A.; Younis, N.A.; Dessouki, A.A.; Maather, M.E.M.M.; Abu Mhara, A.A. & Abdelsalam, M. 2020. Myxobolus episquamalis infection in farmed flathead grey mullet Mugil cephalus L. and thin-lipped mullet Liza ramada. Aquaculture International 28: 363-376.
Fall, M.; Fomena, A.; Kostoingué, B.; Diebakate, C.; Faye, N. & Toguebaye, B.S. 2000. Myxosporidies (Myxozoa, Myxosporea) parasites des poissons Cichlidae du Cameroun, du Sénégal et du Tchad avec la description de deux nouvelles espéces. Annales des Sciences Naturelles-Zoologie et Biologie 21: 81-92.
Feist, S.W. & Longshaw, M. 2006. Phylum myxozoa. In: Woo, P.T.K. (ed.), Fish Diseases and Disorders. Protozoan and Metazoan Infections. CAB International, Oxfordshire. pp: 230-296.
Fomena, A. & Bouix, G. 1997. Myxosporea (Protozoa: Myxozoa) of freshwater fishes in Africa: keys to genera and species. Systematic Parasitology 37: 161-178.
Gómez, D.; Bartholomew, J. & Sunyer, J.O. 2014. Biology and mucosal immunity to Myxozoans. Developmental and Comparative Immunology 43: 243-256.
Gonzalez, S.F.; Buchmann, K. & Nielsen, M.E. 2007. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: Inflammatory responses caused by the ectoparasite Ichthyophthirius multifiliis. Fish & Shellfish Immunology 22: 641-650.
Heinecke, R.D. & Buchmann, K. 2013. Inflammatory response of Rainbow trout Oncorhynchus mykiss (Walbaum, 1792) larvae against Ichthyophthirius multifiliis. Fish & Shellfish Immunology 34: 521-528.
Hutson, J.C. 1993. Secretion of tumor necrosis factor alpha by testicular macrophages. Journal of Reproductive Immunology 23: 63-72.
Kaur, H. & Gupta, A. 2015. Genetic relatedness provides support for a species complex of myxosporeans infecting the Indian major carp, Labeo rohita. Animal Biology 65: 337-347.
Khaled, A.S.A.; Mohammed, A.A.; Thabit, S.; Abdel Azeem, A. & Fathy A.A. 2000. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some River Nile fish, Egypt. Parasitology International 49: 131-137.
Lindenstrøm, T.; Buchmann, K & Secombes, C.J. 2003. Gyrodactylus derjavini infection elicits IL-1ß expression in rainbow trout skin. Fish & Shellfish Immunology 15: 107-115.
Martinus, M.L.; Marchiori, N.; Noumbedakis, K. & Lami, F. 2012. Trichodina nobilis Chen, 1963 and Trichodina reticulate Hirschmann et partsch, 1955 from ornamental freshwater fishes in Brazil. Brazilian Journal of Biology 72: 281-286.
Mohammed, N.I.; Rabie, S.A.; Hussein, A.N.A. & Husssein, N.M. 2012. Infestation of Oreochromis niloticus and Tilapia zilli fresh-water fishes with myxosporean parasites, Qena province, Egypt. Egypt. Academic Journal of Biological Science 4: 235-246.
Mandira, S. & Bandyopadhyay, P.K. 2017. Seasonal incidence of protozoan parasitic infestation in ornamental fishes of West Bengal, India. Journal of Parasitic Disease 41: 523-526.
Ozer, A. & Erdem, O. 1998. Ectoparasitic protozoa fauna of the common carp (Cyprinus carpio L., 1758) caught in the Sinop region of Turkey. Journal of Natural History 32: 441-454.
Ozer, A. & Erdem, O. 1999. The relationship between occurrence of ectoparasites, temperature and culture conditions: A comparison of farmed and wild common carp (Cyprinus carpio L. 1758) in the Sinop region of northern Turkey. Journal of Natural History 33: 483-491.
Ozer, A. 2000. The occurrence of three species of Trichodina (Ciliophora: Peritrichia) on Cyprinus carpio in relation to culture conditions, seasonality and host characteristics. Acta Protozologica 39: 61-66.
Ozer, A. 2003. The occurrence of Trichodina domerguei Wallengren, 1897 and Trichodina tenuidens Faure-Fremiet, 1944 on three spined stickleback, Gasterosteus aculeatus L, 1758 found in a brackish and freshwater environment. Acta Protozologica 42: 41-46.
Ozer, A. 2003. Trichodina domerguei Wallengren, 1897 (Ciliophora: Peritrichia) Infestations on the Round Goby, Neogobius melanostomus Pallas, 1811 in relation to seasonality and host factors. Comparative Parasitology 70: 132-135.
Ovington, K.S.; Alleva, L.M.; & Kerr E.A. 1995. Cytokines and immunological control of Eimeria spp. International Journal of Parasitology 25: 1331-1351.
Ovington, K.S. & Smith N.C. 1992. Cytokines, free radicals and resistance to Eimeria. Parasitology Today 8: 422-426.
Picard-Sanchez, A.; Itziar, E.; Raquel, D.P.M.; Carla, P.; Oswaldo, P. & Ariadna, S.B. 2019. Acquired protective immune response in a fish-myxozoan model encompasses specific antibodies and inflammation resolution. Fish & Shellfish Immunology 90: 349-362.
Praveen, K.; Evans, D.L. & Jaso-Friedmann, L. 2006. Constitutive expression of tumor necrosis factor-alpha in cytotoxic cells of teleosts and its role in regulation of cell-mediated cytotoxicity. Molecular Immunology 43: 279-291.
Saha, M. & Bandyopadhyay, P.K. 2017. Parasitological and histological analysis of a new species of the genus Thalohanellus and description of a myxozoan parasite (Myxosporea: Bivalvulida) from cultured ornamental goldfish, Carassius auratus L. Aquaculture Reports 8: 8-15.
Simon, R.M.J. 2001. The occurrence and mechanisms of innate immunity against parasites in fish. Developmental and Comparative Immunology 25: 841-852.
Sigh, J.; Lindenstrom, T. & Buchmann, K. 2004a. Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophthirius multifiliis. Fish & Shellfish Immunology 7: 76-86.
Sigh, J.; Lindenstrom, T. & Bbuchmann, K. 2004b. The parasitic ciliate Ichthyophthirius multifliis induces expression of immune relevant genes in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 27: 409-417.
Smyth, J.D. 1994. Introduction to Animal Parasitology, 3rd Edition. Cambridge University Press, Cambridge.
Tantry, T.A.; Nazir, R.; Chishti, M.Z.; Ahmad, F.; Dar, G.H. & Dar, J.S. 2016. A report on the incidence of Trichodina heterodentata from fishes of Jammu, J & K, India. Journal of Parasitic Disease 40: 524-527.
Valladao, G.M.R.; Padua, S.B.; Gallani, S.U.; Menezes-filho, R.N.; Dias Neto, J.; Martins, M.L.; Ishikawa, M.M. & Pilarski, F. 2013. Paratrichodina africana (Ciliophora): A pathogenic gill parasite in farmed Nile tilapia. Veterinary Parasitology 197: 705-710.
Valladao, G.M.R.; Alves, L.O. & Pilarski, F. 2016. Trichodiniasis in Nile tilapia hatcheries: Diagnosis, Parasite: host-stage relationship and treatment. Aquaculture 451: 444-450.
Van As, J.G. & Basson, L. 1992. Trichodinid ectoparasites (Ciliophora: Peritrichida) of freshwater fishes of the Zambesi River System, with a reappraisal of host specificity. Systematic Parasitology 22: 81-109.
Wanderson, P.M.F.; Ligia, N.R.; Marcia Dias, R.D.; Renata Marinho, G.B.; Daniel, M. & Marcos, T.D. 2012. Protozoan and metazoan parasites of Nile tilapia oreochromis niloticus cultured in Brazil. Revista MVZ Córdoba 17: 2812-2819.
Wang, Q.; Yongyao, Y.; Xiaoting & Zhen X. 2019 Immune responses of fish to Ichthyophthirius multifiliis (Ich): A model for understanding immunity against protozoan parasites. Developmental and Comparative Immunology 93: 93-102.
Younis, N.A.; Laban, S.E.; Al-Mokaddem, A.K. & Attia, M.M. (2020) Immunological status and histopathological appraisal of farmed Oreochromis niloticus exposed to parasitic infections and heavy metal toxicity. Aquaculture International 28: 1-16.
Zhu, L.; Li, N.; Guan Z.; Li-xin, X. & Jian-zhong, S. 2013. Advances in research of fish immune-relevant genes: A comparative overview of innate and adaptive immunity in teleosts. Developmental and Comparative Immunology 39: 39-62.
Abdel-Azeem, S.A.; Heba, M.A.; Thabet, S.; Eman, Z.; Khalid, E.I. & Al-Quraishy, S. 2015. Two Myxobolus spp. infecting the kidney of Nile tilapia (Oreochromis niloticus) in the River Nile at Beni-Suef governorate, Egypt, and the associated renal changes. Parasitology Research 114: 1107-1112.
Abbas, A.Y.; Abd El-tawab, F.G. & Ebtsam, A.A.T. 2009. Studies on some prevailing parasites affecting Oreochromis niloticus fingerlings with atrial of treatment. Egypt Journal of Aquatic Biology and Fish 13: 135-148.
Akbari, M. & Taghizadeh, V.; Heidarieh, M. & Hajimoradloo, A. 2017. The key role of Tumor Necrosis Factor alpha (TNF-α) in vaccinated rainbow trout via irradiated Ichthyophthirius multifiliis trophont. Veterinary Archive 87: 229-237.
Al-Rasheid, K.A.; Ali, M.A.; Sakran, T.; Baki, A.A.A. & Ghaffar, F.A.A. 2000. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some River Nile fish, Egypt. Parasitology International, 49(2): 131-137.
Attia, M.M.; El-Gameel, S.M. & Ismael, E. 2020. Evaluation of tumor necrosis factor-alpha (TNF-α); gamma interferon (IFN-γ) genes and oxidative stress in sheep: immunological responses induced by Oestrus ovis (Diptera: Oestridae) infestation. Journal of Parasitic Disease 44: 332-337.
Basson, L. & Van As, J.G. 1994. Trichodinid (Ciliophora: Peritrichia) from a calanoid copepod and catfish from South Africa and notes on host specificity. Systematic Parasitology 18: 147-158.
Ben-David, J.; Atkinson, S.D.; Pollak, Y.; Yossifon, G.; Shavit, U.; Bartholomew, J.L.; Lotan, T. 2016. Myxozoan polar tubules display structural and functional variation. Parasite and Vectors 9: 1-6.
Carriero, M.M.; Adriano, E.A.; Silva, M.R.M.; Ceccarelli, P.A. & Maia, A.A.M. 2013. Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLOS One 8: e73713.
Dickerson, H.W. 2012. Ichthyophthirius multifiliis. In: Patrick, K.B. & Woo, T.K. (eds.), Fish Parasites: Pathobiology and Protection. CABI, Wallingford. Pp: 55-72.
Eissa, A.E.; Said, K.A.; Younis, N.A.; Dessouki, A.A.; Maather, M.E.M.M.; Abu Mhara, A.A. & Abdelsalam, M. 2020. Myxobolus episquamalis infection in farmed flathead grey mullet Mugil cephalus L. and thin-lipped mullet Liza ramada. Aquaculture International 28: 363-376.
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