Carrageenin induced inflammation in Piaractus mesopotamicus (Osteichthyes: Characidae) cultured in Brazil
Keywords:
Piaractus mesopotamicus, inflammation, carrageenin, consecutive stress, cortisol, glucose, hematologyAbstract
The present work evaluated the acute inflammatory response induced by carrageenin (500 µg) injection into the swim bladder of pacu (Piaractus mesopotamicus) after consecutive stress of capture. Fish were subjected to air exposition of 30 seconds repeatedly at 60 minutes intervals over six hours. The cellular inflammatory component was evaluated six hours after either the carrageenan or the control (saline injection) by total and differential counts. Cortisol and glucose were analyzed each hour. In the inflammatory exudate, thrombocytes were the most frequently observed cells, followed by macrophages. A significant reduction of cortisol levels was observed after the third stress of capture, as well as an increase in glucose after the second stimulus of stress. Differential counts of circulating leucocytes and thrombocytes show increased percentage of special granulocytic cells and a significant neutrophilia in stressed fish. Non-stressed fish injected with carrageenin presented neutrophilia and lymphopenia. In the swim bladder, carrageenin provoked congestion, interstitial hemorrhage, dissociation of the collagen sheaf and inflammatory infiltrate.
References
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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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