Inflamação aguda provocada por carragenina em pacu, Piaractus mesopotamicus (Osteichthyes: Characidae), cultivado no Brasil
Palavras-chave:
Piaractus mesopotamicus, inflamação, carragenina, estresse consecutivo, cortisol, glicemia, hematologiaResumo
Este trabalho avaliou a resposta inflamatória aguda induzida por injeção de carragenina (500 µg) na bexiga natatória de pacu (Piaractus mesopotamicus) após estresse consecutivo de captura. Os animais foram submetidos a exposição fora da água por 30 segundos, repetindo-se o processo a cada 60 minutos num período de seis horas. Seis horas depois das injeções de solução salina (controle) ou carragenina, o componente da resposta inflamatória foi analisado pela contagem total e diferencial de células. O cortisol e a glicemia foram analisados a cada hora. A análise do exsudato inflamatório mostra predominí¢ncia de trombócitos, seguidos por macrófagos. Significativa redução dos níveis de cortisol observa-se nos animais após o terceiro estímulo estressante, bem como aumento da glicemia após o segundo estímulo. A contagem diferencial de leucócitos e trombócitos circulantes mostra maior porcentagem de células granulocíticas especiais e significativa neutrofilia após o estresse. Os animais que receberam injeção de carragenina apresentaram neutrofilia e linfocitopenia. Na bexiga natatória, a injeção de carragenina provocou congestão, hemorragia intersticial, dissociação dos feixes de colágeno e infiltrado inflamatório.
Referências
BARCELLOS, L.J.G.; WOEHL, V.M.; WASSERMANN,G.F.; QUEVEDO, R.M.; ITTZÉS, I.; KRIEGER, M.H. 2001 Plasma levels of cortisol and glucose in response to capture and tank transference in Rhamdia quelen (Quoy and Gaimard), a South American catfish. Aquac. Res., Oxford, 32: 121-123.
BARCELLOS, L.J.G.; KREUTZ, L.C.; SOUZA, C.; RODRIGUES, L.B.; FIOREZE, I.; QUEVEDO, R.M.; CERICATO, L.; SOSO, A.B.; FAGUNDES, M. CONRAD, L.; LACERDA, L.A.; TERRA, S. 2004 Hematological changes in jundiá (Rhamdia quelen Quoy and Gaimard, Pimelodidae) after acute and chronic stress caused by usual aquacultural management, with emphasis on immunosuppressive effects. Aquaculture,Amsterdam, 237: 229-236.
CECH JR., J.J.; BARTHOLOW, S.D.; YOUNG, P.S.; HOPKINS, T.E. 1996 Striped bass exercise and handling stress in freshwater: physiological responses to recovery environment. Trans. Am.Fish. Soc., Bethesda, 125: 308-320.
CHEN, S.C.; YOSHIDA, T.; ADAMS, A.; THOMPSON, K.D.; RICHARDS, R.H. 1998 Non-specific immune response of Nile tilapia, Oreochromis nilotica, to the extracellular products of Mycobacterium spp and to various adjuvants.
J. Fish Dis., Stirling, 21: 39-46.
CHONDAR, S.L. 1982 The haematology of Gudusia chapra (Pisces: Clupeidae). J. Inland Fish. Soc.India, 14: 1-10.
DIAS, J.L.C. and SINHORINI, I.L. 1991 Qualitative evaluation of the inflammatory response modulated by temperature in tadpoles of Rana catesbeiana. Ci. e Cult., São Paulo, 43: 304-306.
ELLSAESSER, C.F. and CLEM, L.W. 1986 Haematological and immunological changes in channel catfish stressed by handling and transport. J. Fish Biol., London, 28: 511-521.
ENDO, M.; YOSHIDA, T.; SAKAI, M.; IIDA, T. 1995 Swim bladder as a site for administration of chemical agents: application to fish immunology. Fish and Shellfish Immunol., Aberdeen, 5: 85-88.
FARSKY, S.P.; SANNOMIYA, P.; GARCIA LEME, J. 1995 Secreted glucocorticoids regulate leukocyte-endothelial interactions in inflammation. A direct vital microscopic study.J. Leuk. Biol., New York, 57: 379-386.
FEVOLDEN, S.E.; REFSTIE T.; ROED, K.H. 1992 Disease resistance in rainbow trout (Oncorhynchus mykiss) selected for stress response. Aquaculture, Amsterdam, 104: 19-29.
FINN, J.P. 1970 The protective mechanisms in diseases of fish. Vet. Bull., Farnham Royal, 40:873-886.
FINN, J.P. and NIELSEN, N.O. 1971a The effect of temperature variation on the inflammatory response of rainbow trout. J. Pathol., Sussex, 105: 257-268.
FINN, J.P. and NIELSEN, N.O. 1971b The inflammatory response of rainbow trout. J. FishBiol., London, 3: 463-478.
GARCIA LEME, J. 1989 Hormones and Inflammation. Boca Raton: CRC Press. 238p.
GARCIA LEME, J. and SHAPOVAL, E.E.S. 1975 Stimulation of the hypothalamic-pituitaryadrenal axis by compounds formed in inflamed tissue. Braz. J. Pharm. Sci., São Paulo, 53: 75-83.
GRECCHI, R.; SALIBA, A.M.; MARIANO, M. 1980 Morphological changes, surface receptors and phagocytic potencial of fowl mononuclear phagocytes and trombocytes in vivo and in vitro.J. Pathol., Sussex, 130: 23-31.
GRIFFIN, B.R. 1983 Opsonic effect of rainbow trout (Salmo gairdneri) antibody on phagocytosis of Yersinia ruckeri by trout leukocytes. Dev. Comp.Immunol., New York, 7: 253-259.
HOUSTON, A.H.; DOBRIC, N.; KAHURANANGA, R.1996 The nature of hematological response in fish. Fish Physiol. Biochem., Amsterdam, 15:339-347.
JAKOWSKA, S. and NIGRELLI, R.F. 1953 Localized response to experimental inflammation caused by pathogenic bacteria. Anat. Rec., New York, 117: 526.
JENKINS, J.A. and KLESIUS, P.H. 1998 Elicitation of macrophages from the peritoneal cavity of channel catfish. J. Aquat. Anim. Health, Bethesda, 10: 69-74.
KAJIGAYA, H.; KAMEKURA, M.; TANAHARA, N.;OTHA, A.; SUZUKI, H.; SUGIYAMA, M.; ISODA, M. 1985 Acute and chronic inflammation induced by silk sutures in chicken mesentery. Bull. Nippon Vet. Zoot. Coll., Japan, 34: 35-38.
KING, E.J. and GARNER, R.J. 1947 Colorimetric determination of glucose. J. Clin. Pathol.,London, 1: 30-33.
KLUGE, J.P. 1965 A granulomatous disease of fish produced by flavobacteria. Pathology and Veterinary, Washington, 2: 545-552.
KOVÁCS-GAYER, É. 1983 Histopathological studies on protozoon swimbladder inflammation of commom carp fry. Parazitologia Hungarica, Budapest, 16: 39-46.
KRIEGER-AZZOLINI, M.H.; DELATTRE, E.; CARLSFELD, J.; CECCARELLI, P.S.; MENEZES, F.V. 1989 A time-course study of phisiological indicators of handling stress in the tropical fish Piaractus mesopotamicus (Pacu). Braz. J. Med. Biol. Res., Ribeirão Preto, 22: 1019-1022.
LEA MASTER, B.R.; BROCK, J.A.; FUJIOKA, R.S.; NAKAMURAS, R.M. 1990 Hematologic and blood chemistry values for Sarotherodon melanotheron and a red hybrid tilapia in freshwater and seawater. Comp. Biochem.Physiol., Oxford, 97A: 525-529.
MACARTHUR, J.I.; FLETCHER, T.C.; PIRIE, B.J.S.; DAVIDSON, R.J.L.; THOMSON, A.W. 1984 Peritoneal inflammatory cells in plaice, Pleuronectes platessa L.: effects of stress and endotoxin. J. Fish Biol., London, 25: 69-81.
MARTINS, M.L.; MORAES, F.R.; MORAES, J.R.E.; MALHEIROS, E.B. 2000 Falha na resposta do cortisol ao estresse por captura e por carragenina em Piaractus mesopotamicus Holmberg, 1887 (Osteichthyes: Characidae). Acta Scientiarum,Maringá, 22: 545-552.
MARTINS, M.L.; PILARSKY, F.; ONAKA, E.M.; NOMURA, D.T.; FENERICK Jr., J.; RIBEIRO, K.; MYIAZAKI, D.M.Y.; CASTRO, M.P.; MALHEIROS, E.B. 2004 Hematologia e resposta inflamatória aguda em Oreochromis
niloticus (Osteichthyes: Cichlidae) submetida aos estímulos único e consecutivo de estresse de captura. B. Inst. Pesca, São Paulo,30(1): 71-80.
MATUSHIMA, E.R. and MARIANO, M. 1996 Kinetics of the inflammatory reaction induced by carrageenin in the swimbladder of Oreochromis niloticus (Nile tilapia). Braz. J. Vet.Res. Anim. Sci., São Paulo, 33: 5-10.
MAULE, A.G.; TRIPP, R.A.; KAATTARI, S.L.; SCHRECK, C.B. 1989 Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha).J. Endocrinol., Bristol, 120: 135-142.
MCCORMICK, S.D.; SHRIMPTOM, J.M.; CAREY, J.B.; O´DEA, M.F.; SLOAN, K.E.; MORIYAMA, S.; BJí–RNSSON, B.T. 1998 Repeated acute stress reduces growth rate of Atlantic samon parr and alters plasma levels of growth hormone, insulinlike growth factor 1 and cortisol. Aquaculture, Amsterdam, 168: 221-235.
MCDONALD, G. and MILLIGAN, L. 1997 Ionic, osmotic and acid-base regulation in stress. In: IWANA, G.W.; PICKERING, A.D.; SUMPTER,J.P.; SCHRECK, C.B. (Ed.). Fish stress and health in aquaculture. Cambridge: Unniversity Press. p.119-144.
MESNILL, F. 1895 Sur le mode des resistance des vertebrades inferieures aux invasions microfiennes. Ann. Inst. Pasteur, Paris, 2: 301-311.
METCHNIKOFF, E. 1905 Immunity in Infective Diseases. Cambridge: University Press.
MORAES, F.R. and GARCIA LEME, J. 1982 Endogenous corticosteroids and insulin in the acute inflammation. Microv. Res., San Diego, 23: 281-93.
MORAES, F.R.; BECHARA, G.H.; MORAES, J.R.E.1987 Effect of alloxan diabetes and adrenalectomy on carrageenin-induced pleurisy in the rat. Braz. J. Med. Biol. Res., Ribeirão Preto, 20: 47-53.
MURRAY, S.A. 1984 Hematological study of the bluegill, Lepomis macrochirus Raf. Comp. Biochem.Physiol., Oxford, 78A: 787-791.
NARNAWARE, Y.K. and BAKER, B.I. 1996 Evidence that cortisol may protect against the immediate effects of stress on circulating leukocytes in the trout. Gen. Comp. Endocrinol.,San Diego, 103: 359-366.
PAULSEN, S.M.; ENGSTAD, R.E.; ROBERTSEN, B. 2001 Enhanced lysozyme production in Atlantic salmon (Salmo salar L.) macrophages treated with yeast í¢-glucan and bacterial lipopolysaccharide. Fish and Shellfish Immunol., Aberdeen, 11: 23-37.
POST, G. 1963 The imune response of rainbow trout to Aeromonas hydrophila. Utah State Dep.Fish and Game, Utah, 62-67: 1-82.
REZNIKOFF, P. and REZNIKOFF, D.G. 1934 Hematological studies in dogfish (Mustelus canis). Biol. Bull. Maric. Biol. Lab. Woods Hole, Massachussets, 66: 115-123.
ROSENFELD, G. 1947 Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do MayGrünwald e do Giemsa num só corante de emprego rápido. Mem. Inst. Butantan, São Paulo,20: 329-334.
SMART, G.R. 1981 Aspects of water quality producing stress in intensive fish culture. In:PICKERING, A.D. (Ed.). Stress and Fish. London: Academic Press. p.277-293.
STEEL, R.G.D. and TORREY, J.H. 1980 Principles and Procedures of Statistics. 2. ed. New York:McGraw Hill. 633p.
SUZUKI, K. 1986 Morphological and phagocytic characteristics of peritoneal exudate cells in tilapia, Oreochromis niloticus (Trewavas), and carp, Cyprinus carpio L. J. Fish Biol., London, 29:349-364.
TAVARES-DIAS, M.; SANDRIM, E.F.S.; MORAES, F.R.; CARNEIRO, P.C.F. 2001 Physiological responses of "tambaqui†Colossoma macropomum (Characidae) to acute stress. B. Inst. Pesca, São Paulo, 27: 43-48.
TIMUR, G.; ROBERTS, R.J.; MCQUEEN, A. 1977 Carrageenin granuloma in the place (Pleuronectes platessa): a histopathological study of chronic inflammation in a teleost fish. J. Comp. Pathol.,Edinburgh, 87: 83-87.
WEINREB, E.L. 1958 Studies on the histology and histopathology of the rainbow trout, Salmo gairdneri irideus. I. Hematology: Under normal and experimental conditions of inflammation.Zoologica, New York, 43: 145-154.
YOKOYAMA, H.; DANJO, T.; OGAWA, K.; ARIMA, T.; WAKABAYASHI, H. 1996 Hemorrhagic anemia of carp associated with spore discharge of Myxobolus artus (Myxozoa: Myxosporea).Fish Pathol., Tokyo, 31: 19-23.
BARCELLOS, L.J.G.; KREUTZ, L.C.; SOUZA, C.; RODRIGUES, L.B.; FIOREZE, I.; QUEVEDO, R.M.; CERICATO, L.; SOSO, A.B.; FAGUNDES, M. CONRAD, L.; LACERDA, L.A.; TERRA, S. 2004 Hematological changes in jundiá (Rhamdia quelen Quoy and Gaimard, Pimelodidae) after acute and chronic stress caused by usual aquacultural management, with emphasis on immunosuppressive effects. Aquaculture,Amsterdam, 237: 229-236.
CECH JR., J.J.; BARTHOLOW, S.D.; YOUNG, P.S.; HOPKINS, T.E. 1996 Striped bass exercise and handling stress in freshwater: physiological responses to recovery environment. Trans. Am.Fish. Soc., Bethesda, 125: 308-320.
CHEN, S.C.; YOSHIDA, T.; ADAMS, A.; THOMPSON, K.D.; RICHARDS, R.H. 1998 Non-specific immune response of Nile tilapia, Oreochromis nilotica, to the extracellular products of Mycobacterium spp and to various adjuvants.
J. Fish Dis., Stirling, 21: 39-46.
CHONDAR, S.L. 1982 The haematology of Gudusia chapra (Pisces: Clupeidae). J. Inland Fish. Soc.India, 14: 1-10.
DIAS, J.L.C. and SINHORINI, I.L. 1991 Qualitative evaluation of the inflammatory response modulated by temperature in tadpoles of Rana catesbeiana. Ci. e Cult., São Paulo, 43: 304-306.
ELLSAESSER, C.F. and CLEM, L.W. 1986 Haematological and immunological changes in channel catfish stressed by handling and transport. J. Fish Biol., London, 28: 511-521.
ENDO, M.; YOSHIDA, T.; SAKAI, M.; IIDA, T. 1995 Swim bladder as a site for administration of chemical agents: application to fish immunology. Fish and Shellfish Immunol., Aberdeen, 5: 85-88.
FARSKY, S.P.; SANNOMIYA, P.; GARCIA LEME, J. 1995 Secreted glucocorticoids regulate leukocyte-endothelial interactions in inflammation. A direct vital microscopic study.J. Leuk. Biol., New York, 57: 379-386.
FEVOLDEN, S.E.; REFSTIE T.; ROED, K.H. 1992 Disease resistance in rainbow trout (Oncorhynchus mykiss) selected for stress response. Aquaculture, Amsterdam, 104: 19-29.
FINN, J.P. 1970 The protective mechanisms in diseases of fish. Vet. Bull., Farnham Royal, 40:873-886.
FINN, J.P. and NIELSEN, N.O. 1971a The effect of temperature variation on the inflammatory response of rainbow trout. J. Pathol., Sussex, 105: 257-268.
FINN, J.P. and NIELSEN, N.O. 1971b The inflammatory response of rainbow trout. J. FishBiol., London, 3: 463-478.
GARCIA LEME, J. 1989 Hormones and Inflammation. Boca Raton: CRC Press. 238p.
GARCIA LEME, J. and SHAPOVAL, E.E.S. 1975 Stimulation of the hypothalamic-pituitaryadrenal axis by compounds formed in inflamed tissue. Braz. J. Pharm. Sci., São Paulo, 53: 75-83.
GRECCHI, R.; SALIBA, A.M.; MARIANO, M. 1980 Morphological changes, surface receptors and phagocytic potencial of fowl mononuclear phagocytes and trombocytes in vivo and in vitro.J. Pathol., Sussex, 130: 23-31.
GRIFFIN, B.R. 1983 Opsonic effect of rainbow trout (Salmo gairdneri) antibody on phagocytosis of Yersinia ruckeri by trout leukocytes. Dev. Comp.Immunol., New York, 7: 253-259.
HOUSTON, A.H.; DOBRIC, N.; KAHURANANGA, R.1996 The nature of hematological response in fish. Fish Physiol. Biochem., Amsterdam, 15:339-347.
JAKOWSKA, S. and NIGRELLI, R.F. 1953 Localized response to experimental inflammation caused by pathogenic bacteria. Anat. Rec., New York, 117: 526.
JENKINS, J.A. and KLESIUS, P.H. 1998 Elicitation of macrophages from the peritoneal cavity of channel catfish. J. Aquat. Anim. Health, Bethesda, 10: 69-74.
KAJIGAYA, H.; KAMEKURA, M.; TANAHARA, N.;OTHA, A.; SUZUKI, H.; SUGIYAMA, M.; ISODA, M. 1985 Acute and chronic inflammation induced by silk sutures in chicken mesentery. Bull. Nippon Vet. Zoot. Coll., Japan, 34: 35-38.
KING, E.J. and GARNER, R.J. 1947 Colorimetric determination of glucose. J. Clin. Pathol.,London, 1: 30-33.
KLUGE, J.P. 1965 A granulomatous disease of fish produced by flavobacteria. Pathology and Veterinary, Washington, 2: 545-552.
KOVÁCS-GAYER, É. 1983 Histopathological studies on protozoon swimbladder inflammation of commom carp fry. Parazitologia Hungarica, Budapest, 16: 39-46.
KRIEGER-AZZOLINI, M.H.; DELATTRE, E.; CARLSFELD, J.; CECCARELLI, P.S.; MENEZES, F.V. 1989 A time-course study of phisiological indicators of handling stress in the tropical fish Piaractus mesopotamicus (Pacu). Braz. J. Med. Biol. Res., Ribeirão Preto, 22: 1019-1022.
LEA MASTER, B.R.; BROCK, J.A.; FUJIOKA, R.S.; NAKAMURAS, R.M. 1990 Hematologic and blood chemistry values for Sarotherodon melanotheron and a red hybrid tilapia in freshwater and seawater. Comp. Biochem.Physiol., Oxford, 97A: 525-529.
MACARTHUR, J.I.; FLETCHER, T.C.; PIRIE, B.J.S.; DAVIDSON, R.J.L.; THOMSON, A.W. 1984 Peritoneal inflammatory cells in plaice, Pleuronectes platessa L.: effects of stress and endotoxin. J. Fish Biol., London, 25: 69-81.
MARTINS, M.L.; MORAES, F.R.; MORAES, J.R.E.; MALHEIROS, E.B. 2000 Falha na resposta do cortisol ao estresse por captura e por carragenina em Piaractus mesopotamicus Holmberg, 1887 (Osteichthyes: Characidae). Acta Scientiarum,Maringá, 22: 545-552.
MARTINS, M.L.; PILARSKY, F.; ONAKA, E.M.; NOMURA, D.T.; FENERICK Jr., J.; RIBEIRO, K.; MYIAZAKI, D.M.Y.; CASTRO, M.P.; MALHEIROS, E.B. 2004 Hematologia e resposta inflamatória aguda em Oreochromis
niloticus (Osteichthyes: Cichlidae) submetida aos estímulos único e consecutivo de estresse de captura. B. Inst. Pesca, São Paulo,30(1): 71-80.
MATUSHIMA, E.R. and MARIANO, M. 1996 Kinetics of the inflammatory reaction induced by carrageenin in the swimbladder of Oreochromis niloticus (Nile tilapia). Braz. J. Vet.Res. Anim. Sci., São Paulo, 33: 5-10.
MAULE, A.G.; TRIPP, R.A.; KAATTARI, S.L.; SCHRECK, C.B. 1989 Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha).J. Endocrinol., Bristol, 120: 135-142.
MCCORMICK, S.D.; SHRIMPTOM, J.M.; CAREY, J.B.; O´DEA, M.F.; SLOAN, K.E.; MORIYAMA, S.; BJí–RNSSON, B.T. 1998 Repeated acute stress reduces growth rate of Atlantic samon parr and alters plasma levels of growth hormone, insulinlike growth factor 1 and cortisol. Aquaculture, Amsterdam, 168: 221-235.
MCDONALD, G. and MILLIGAN, L. 1997 Ionic, osmotic and acid-base regulation in stress. In: IWANA, G.W.; PICKERING, A.D.; SUMPTER,J.P.; SCHRECK, C.B. (Ed.). Fish stress and health in aquaculture. Cambridge: Unniversity Press. p.119-144.
MESNILL, F. 1895 Sur le mode des resistance des vertebrades inferieures aux invasions microfiennes. Ann. Inst. Pasteur, Paris, 2: 301-311.
METCHNIKOFF, E. 1905 Immunity in Infective Diseases. Cambridge: University Press.
MORAES, F.R. and GARCIA LEME, J. 1982 Endogenous corticosteroids and insulin in the acute inflammation. Microv. Res., San Diego, 23: 281-93.
MORAES, F.R.; BECHARA, G.H.; MORAES, J.R.E.1987 Effect of alloxan diabetes and adrenalectomy on carrageenin-induced pleurisy in the rat. Braz. J. Med. Biol. Res., Ribeirão Preto, 20: 47-53.
MURRAY, S.A. 1984 Hematological study of the bluegill, Lepomis macrochirus Raf. Comp. Biochem.Physiol., Oxford, 78A: 787-791.
NARNAWARE, Y.K. and BAKER, B.I. 1996 Evidence that cortisol may protect against the immediate effects of stress on circulating leukocytes in the trout. Gen. Comp. Endocrinol.,San Diego, 103: 359-366.
PAULSEN, S.M.; ENGSTAD, R.E.; ROBERTSEN, B. 2001 Enhanced lysozyme production in Atlantic salmon (Salmo salar L.) macrophages treated with yeast í¢-glucan and bacterial lipopolysaccharide. Fish and Shellfish Immunol., Aberdeen, 11: 23-37.
POST, G. 1963 The imune response of rainbow trout to Aeromonas hydrophila. Utah State Dep.Fish and Game, Utah, 62-67: 1-82.
REZNIKOFF, P. and REZNIKOFF, D.G. 1934 Hematological studies in dogfish (Mustelus canis). Biol. Bull. Maric. Biol. Lab. Woods Hole, Massachussets, 66: 115-123.
ROSENFELD, G. 1947 Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do MayGrünwald e do Giemsa num só corante de emprego rápido. Mem. Inst. Butantan, São Paulo,20: 329-334.
SMART, G.R. 1981 Aspects of water quality producing stress in intensive fish culture. In:PICKERING, A.D. (Ed.). Stress and Fish. London: Academic Press. p.277-293.
STEEL, R.G.D. and TORREY, J.H. 1980 Principles and Procedures of Statistics. 2. ed. New York:McGraw Hill. 633p.
SUZUKI, K. 1986 Morphological and phagocytic characteristics of peritoneal exudate cells in tilapia, Oreochromis niloticus (Trewavas), and carp, Cyprinus carpio L. J. Fish Biol., London, 29:349-364.
TAVARES-DIAS, M.; SANDRIM, E.F.S.; MORAES, F.R.; CARNEIRO, P.C.F. 2001 Physiological responses of "tambaqui†Colossoma macropomum (Characidae) to acute stress. B. Inst. Pesca, São Paulo, 27: 43-48.
TIMUR, G.; ROBERTS, R.J.; MCQUEEN, A. 1977 Carrageenin granuloma in the place (Pleuronectes platessa): a histopathological study of chronic inflammation in a teleost fish. J. Comp. Pathol.,Edinburgh, 87: 83-87.
WEINREB, E.L. 1958 Studies on the histology and histopathology of the rainbow trout, Salmo gairdneri irideus. I. Hematology: Under normal and experimental conditions of inflammation.Zoologica, New York, 43: 145-154.
YOKOYAMA, H.; DANJO, T.; OGAWA, K.; ARIMA, T.; WAKABAYASHI, H. 1996 Hemorrhagic anemia of carp associated with spore discharge of Myxobolus artus (Myxozoa: Myxosporea).Fish Pathol., Tokyo, 31: 19-23.
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2018-10-29
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