Pathogenicity of vibrios in fish: An overview

Journal of Ocean University of Qingdao - Tập 2 Số 2 - Trang 117-128 - 2003
Jun Li1, Norman Y.S. Woo1
1Department of Biology, The Chinese University of Hong Kong, Shatin, N. T., Hong Kong SAR, P.R. China

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Tài liệu tham khảo

Alcaide, E., C. Amaro, R. Todoli, and R. Oltra, 1999. Isolation and characterization of Vibrio parahaemolyticus causing infection in Iberian toothcarp Aphanius iberus. Dis. Aquat. Org., 35: 77–80.

Alvarez, J. D., B. Austin, A. M. Alvarez, and H. Reyes, 1988. Vibrio harveyi: a pathogen of penaeid shrimps and fish in Venezuela. J. Fish. Dis., 21: 313–316.

Amaro, C., E. G. Biosca, B. Fouz, E. Alcaide, and C. Esteve, 1995. Evidence that water transmimits Vibrio vulnificus biotype 2 infections to eels. Appl. Environ. Microbiol., 61: 1133–1137.

Anderson, D. P., 1990. Immunological indicators: Effects of environmental stress on immune protection and disease outbreaks. Am. Fish. Soc. Sym., 8: 38–50.

Anderson, J. W., and D. A. Conroy, 1970. Vibrio diseases in fishes. In: A Symposium on Diseases of Fishes and Shell-fishes. Snieszko, S. F., ed., American Fisheries Society, Special Publication No. 5, Washington, D. C. 266–272.

Angulo, L., J. E. Lopez, J. A. Vicente, and A. M. Saborido, 1994. Hemorrhagic areas in the mouth of farmed turbot, Scophthalmus maximus L. J. Fish Dis., 17: 163–169.

Aoki, T., J. Nomura, and J. H. Crosa, 1985. Virulence of Vibrio anguillarum with particular emphasis on the outer membrane components. Bull. Japn. Soc. Sci. Fish., 51: 1249–1254.

Austin, B., M. Stobie, P. A. W. Robertson, H. G. Glass, and J. R. Stark, 1993. Vibrio alginolyticus: the cause of gill disease leading to progressive low-level mortalities among juvenile turbot, Scophthalmus maximus L., in a Scottish aquarium. J. Fish. Dis., 16: 277–290.

Austin, B., and D. A. Austin, 1993. Bacterial Fish Pathogens. 2nd edition. Ellis Horwood Ltd., Chichester. pp. 265–307.

Balebona, M. C., M. J. Andreu, M. A. Bordas, I. Zorrilla, M. A. Morinigo, et al., 1998. Pathogenicity of Vibrio alginolyticus for cultured gilthead sea bream (Sparus aurata L.). Appl. Environ. Microbiol., 64: 4269–4275.

Benediktsottir, E., S. Helgason, and H. Sigurjonsdottir, 1998. Vibrio sp. isolated from salmonids with shallow skin lesions and reared at low temperature. J. Fish. Dis., 21: 19–28.

Bertone, S., C. Gili, A. Moizo, and L. Calegari, 1996. Vibrio carchariae associated with a chronic skin ulcer on a shark, Carcharhinus plumbeus (Nardo). J. Fish Dis., 19: 429–434.

Biosca, E. G., and C. Amaro, 1996. Toxic and enzymatic activities of Vibrio vulnificus biotype 2 with respect to host specificity. Appl. Environ. Microbiol., 62: 2331–2337.

Biosca, E. G., C. Amaro, C. Esteve, E. Alcaide, and E. Garay, 1991. First record of Vibrio vulnificus biotype 2 from diseased European eel, Anguilla anguilla L., J. Fish. Dis., 14: 103–109.

Biosca, E., B. Fouz, E. Alcaide, and C. Amaro, 1996. Siderophore-mediated iron acquisition mechanisms in Vibrio vulnificus biotypes 2. Appl. Environ. Microbiol., 62: 928–935.

Bly, J. E., and L. W. Clem, 1992. Temperature and teleost immune function. Fish Shellfish Immunol., 2: 159–171.

Bruno, D. W., J. Griffiths, J. Petrie, and T. S. Hastings, 1998. Vibrio viscous in farmed Atlantic salmon Salmo salar in Scotland: field and experimental observations. Dis. Aquat. Org., 34: 161–166.

Bruno, D. W., T. S. Hastings, and A. E. Ellis, 1986. Histopathology, bacteriology and experimental transmission of cold-water vibriosis in Atlantic salmon Salmo salar. Dis. Aquat. Org., 1: 163–168.

Burke, J., and L. Rodgers, 1981. Identification of pathogenic bacteria associated with the occurrence of ‘red spot’ in sea mullet, Mugil cephalus L. in south eastern Queensland. J. Fish. Dis., 3: 153–159.

Chart, H., 1983. Multiflagellate variants of Vibrio anguillarum J. Gen. Microbiol., 129: 2193–2197.

Chart, H., and T. J. Trust, 1984. Characterization of the surface antigens of the marine fish pathogens, Vibrio anguillarum and Vibrio ordalii. Can. J. Microbiol., 30: 703–710.

Collado, R., B. Fouz, E. Sanjuan, and C. Amaro, 2000. Effectiveness of different vaccine formulations against vibriosis caused by Vibrio vulnificus serovarE (biotype 2) in European eels Anguilla anguilla. Dis. Aquat. Org., 14: 91–101.

Colorni, A., I. Paperna, and H. Gordin, 1981. Bacterial infections in gilt-head sea brean Sparus aurata cultured at Elat. Aquaculture, 23: 257–267.

Colwell, R. R., and D. J. Griems, 1984. Vibrio diseases of marine fish populations. Helgölander Meeresunters, 37: 265–287.

Conchas, R. F., M. L. Lemos, J. L. Barja, and A. E. Toranzo, 1991. Distribution of plasmid- and chromosome-mediated iron uptake system in Vibrio anguillarum strains of different origins. Appl. Environ. Microbiol., 57: 2956–2962.

Crosa, J. H., 1980. A plasmid associated with virulence in the marine fish pathogen Vibrio anguillarum species an iron-sequestering system. Nature, 283: 566–568.

Crosa, J. H., 1984. The relationship of plasmid-mediated iron transport and bacteria virulence. Ann. Rev. Microbiol., 38: 69–89.

Dalmo, R. A., K. Ingebrigtsen, and J. Bogwald, 1997. Non-specific defense mechanisms in fish, with particular reference to the reticuloendothelial system (RES). J. Fish. Dis., 20: 241–273.

Dalsgaard, I., L. Hoi, R. J. Siebeling, and A. Dalsgaard, 1999. Indole-positive Vibrio vulnificus isolated from disease outbreaks on a Danish eel farm. Dis. Aquat. Org., 35: 187–194.

De la Cruz, M. C., and K. Muroga, 1989. The effects of Vibrio anguillarum extracellular products on Japanese eels. Aquaculture, 80: 201–210.

Deane, E. E., Li, J., and N. Y. S. Woo, 2001. Hormonal status and phagocytic activity of sea bream infected with vibriosis. Comp. Biochem. Physiol., 129B: 687–693.

Diggles, B. K., J. Carson, P. M. Hine, R. W. Hickman, and M. J. Tait, 2000. Vibrio species associated with mortalities in hatchery-reared turbot (Colistium mudipinnis) and brill (C. guntheri) in New Zealand. Aquaculture, 183: 1–12.

Egidius, E., 1987. Vibriosis: pathogenicity and pathology. A review. Aquaculture, 67: 15–28.

Espelid, S., K. Hjelmeland, and T. Jorgensen, 1987. The specificity of Atlantic salmon antibodies made against the fish pathogen Vibrio salmonicida, establishing the surface protein VS-P1 as the dominating antigen. Dev. Comp. Immunol., 11: 529–537.

Esteve, C., C. Amaro, E. G. Biosca, and E. Garay, 1995. Biochemical and toxigenic properties of Vibrio furnissii isolated from a European eel farm. Aquaculture, 132: 81–90.

Evenberg, D., P. de Graff, W. Fleuren, and W. B. Van Muiswinkel, 1986. Blood changes in carp (Cyprinus corpio) induced by ulcerative Aeromonas salmonicida infections. Vet. Immunol. Immunopathol., 12: 321–330.

Farkas, J., and S. E. Malik, 1986. Vibrio diseases of sheat-fish (Silurus glanis L.) fry. Aquaculture, 51: 81–88.

Farto, R., M. J. Perez, A. Fernandez-Briera, and T. P. Nieto, 2002. Purification and partial characterization of a fish lethal extracellular protease from Vibrio pelagius. Vet. Microbiol., 89: 181–194.

Fouz, B., J. L. Barja, C. Amaro, C. Rivas, and A. E. Toranzo, 1992a. Toxicity of extracellular products of Vibrio damsela isolated from diseased fish. Curr. Microbiol., 27: 341–347.

Fouz, B., S. Devesa, K. Gravningen, J. L. Barja, and A. E. Toranzo, 1990. Antibacterial action of the mucus of turbot. Bull. Eur. Ass. Fish Pathol., 10: 56–59.

Fouz, B., J. L. Larsen, B. Nielsen, J. L. Barja, and A. E. Toranzo, 1992b. Characterization of Vibrio damsela strains isolated from turbot Scophthalmus maximus in Spain. Dis. Aquat. Org., 12: 155–166.

Fouz, B., B. Novoa, A. E. Toranzo, and A. Figuras, 1995. Histopathological lesions caused by Vibrio damsela in cultured turbot, Scophthalmus maximus (L.): inoculations with live cells and extracellular products. J. Fish Dis., 18: 357–364.

Fouz, B., A. E. Toranzo, E. G. Biosca, R. Mazoy, and C. Amaro. 1994. Role of iron in the pathogenicity of Vibrio damsela for fish and animals. FEMS Microbiol. Lett., 121: 181–188.

Fouz, B., A. E. Toranzo, M. Milan, and C. Amaro, 2000. Evidence that water transmits the disease caused by the fish pathogen Photobacterium damsela subsp damsela. J. Appl. Microbiol., 88: 531–535.

French, G. L., M. L. Woo, Y. W. Hui, and K. Y. Chan, 1989. Antimicrobial susceptibilities of halophilic vibrios. J. Antimicrob. Chemother., 24: 183–194.

Greger, E., and T. Goodrich, 1999. Vaccine development for winter ulcer disease, Vibrio viscosus, in Atlantic salmon, Salmo salar L. J. Fish. Dis., 22: 193–199.

Grimes, D. J., H. Stemmier, E. B. May, D. Maneval, F. M. Hetrick, et al., 1984. Vibrio species associated with mortality of sharks held in captivity. Microb. Ecol., 10: 271–282.

Grimes, D. J., S. H. Gruber, and E. B. May, 1985. Experimental infection of lemon sharks, Negaprion brevirostris (Poey), with Vibrio species. J. Fish Dis., 8: 173–180.

Haney, D. C., D. A. Hursh, M. C. Mix, and J. R. Winton, 1992. Physiological and hematological changes in chum salmon artificially infected with erythrocyte necrosis virus. J. Aquat. Anim. Health, 4: 48–57.

Harrel, L. W., H. M. Etlinger, and H. O. Hodgins, 1976. Humoral factors important in resistance of salmonid fish to bacterial disease. II. Anti-V. anguillarum activity in mucus and observation on complement. Aquaculture, 7: 363–370.

Harris, J., and D. J. Bird, 2000. Modulation of the fish immune system by hormones (Mini review). Vet. Immunol. Immunopathol., 77: 163–176.

Hedrick, R. P., 1998. Relationships of the host, pathogen, and environment: Implications for diseases of cultures and wild fish populations. J. Aquat. Anim. Health, 10: 107–111.

Hjelmeland, K., K. Stensvag, T. Jorgensen, and S. Espelid, 1988. Isolation and characterization od a surface layer antigen from Vibrio salmonicida. J. Fish. Dis., 10: 85–90.

Hoff, K. A., 1989. Survival of Vibrio anguillarum and Vibrio salmonicida at different salinities. Appl. Environ. Microbiol., 55: 1775–1786.

Horne, M. T., and A. Baxendale, 1983. The adhesion of Vibrio anguillarum to host tissues and role in pathogenesis. J. Fish Dis., 6: 461–471.

Hou, Y. Y., Y. Suzuki, and K. Aida, 1999. Effects of steroid hormones on immunoglobulin M (IgM) in rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem., 20: 155–162.

Inamura, H., K. Muroga, and T. Nakai, 1984. Toxicity of extracellular products of Vibrio anguillarum. Fish Pathol., 22: 153–158.

Inamura, H., T. Nakai, and K. Muroga, 1985. An extracellular protease produced by Vibrio anguillarum. Bull. Jap. Soc. Sci. Fish., 51: 1915–1920.

Iwama, G. K., G. L. Greer, and D. J. Randall, 1986. Changes in selected hematological parameters in juvenile Chinook salmon subjected to bacterial challenge and a toxicant. J. Fish. Biol., 28: 563–572.

Iranto, A., and B. Austin, 2002. Probiotics in aquaculture. J. Fish Dis., 25: 633–642.

Jensen, S., O. B. Samuelsen, K. Andersen, L. Torkildsen, and C. Lambert, 2003. Characterization of strains of Vibrio splendidus and V. tapetis isolated from corkwing wrasse Symphodus melops suffering vibriosis. Dis. Aquat. Org., 53:25–31.

Kanno, T., T. Nakai, and K. Muroga, 1989. Mode of transmission of vibrosis among ayu, Plecoglossus altivelis. J. Aquat. Anim. Health. 1: 2–6.

Lamas, J., Y. Santos, D. Bruno, A. E. Toranzo, and R. Anadon, 1994. A comparison of pathological changes caused by Vibrio anguillarm and its extracellular products in rainbow trout (Oncorhynchus mykiss). Fish Pathol., 29: 79–89.

Lee, K. K., 1995. Pathogenesis studies on Vibrio alginolyticus in the grouper, Epinephelus malabaricus, Bloch et Schneider. Microb. Pathol., 19: 39–48.

Lee, K. K., P. C. Liu, and W. H. Chuang, 2002, Pathogenesis of gastroenteritis caused by Vibrio carchariae in cultured marine fish. Mar. Biotechnol, 4: 267–277.

Lee, K. K., and K. C. Yii, 1996. A comparison of three methods for assaying hydrophobicity of pahtogenic vibrios. Lett. Appl. Microbiol., 23: 343–346.

Lemos, M. L., P. Salinas, A. E. Toranzo, J. L. Barja, and J. H. Crosa, 1988. Chromosome-mediated iron-uptake systems in Vibrio anguillarum. J. Bacteriol., 170: 1920–1925.

Li, J., 2002. Vibrio alginolyticus: Pathogenicity and Its Immunological Control via Vaccination in Silver Sea Bream, Sparus sarba. Ph.D. thesis. The Chinese University of Hong Kong, Hong Kong.

Li, J., Feng, F., Liu, X., Li, Q. F., N. Y. S. Woo, et al., 1998. Vibrio alginolyticus, a pathogen of silver sea bream, Sparus sarba, cultured in Hong Kong. J. Fish. China, 22: 275–278.

Li, J., J. Yie, R. W. T. Foo, J. M. L. Ling, H. Xu, et al., 1999. Antibiotic resistance and plasmid profiles of vibrio isolates from cultured silver sea bream, Sparus sarba. Mar. Pollut. Bull., 39: 245–249.

Liu, X. Z., Zou, X. L., Mo, X. Y., Li, J. B., Ye, Z. T., et al., 1994. Studies on the pathogenic bacteria of Epinephyelus sp. in marine cage culture. Trop. Oceanol., 13: 81–85 (in Chinese).

Love, M., D. T. Fiher, J. E. Hose, J. J. Farmer, F. W. Hickman, et al., 1981. Vibrio damsela, as a marine bacterium causes skin ulcers on the damselafish Chromis punctipinnis. Science, 214: 1140–1141.

Lunder, T., O. Evensen, G. Holstad, and T. Hastein, 1995. Winter ulcer in the Atlantic salmon, Salmo salar. Pathological and bacteriological investigations and transmission experiments. Dis. Aquat. Org., 23: 39–40.

Magarinos, B., N. Couso, M. Noya, P. Merino, A. E. Toranzo, et al., 2001. Effect of temperature on the development of pasteurellosis in carrier gilthead seabream, Sparus aurata. Aquaculture, 195: 17–21.

Magnadottir, B., and B. K. Gudmundsdottir, 1992. A comparison of total and specific immunoglobulin levels in healthy Atlantic salmon (Salmo salar L.) and in salmon naturally infected with Aeromonas salmonicida subsp. achromogenes. Vet. Immunol. Immunopathol., 32: 179–189.

Magnadottir, B., H. Jonsdottir, S. Helgason, B. Biornsson, T. O. Jorgensen, et al., 1999. Humoral immune parameters in Atlantic cod (Gadus morhua L.) I: The effects of environmental temperature. Comp. Biochem. Physiol., 122B: 173–180.

Mahoney, J. B., and J. K. McNulty, 1992. Disease-associated blood changes and normal seasonal hematological variation in winter flounder in the Hudson-Raritan estuary. Trans. Am. Fish. Soc., 121: 261–268.

Marco-Noales, E., M. Milan, B. Fouz, E. Sanjuan, and C. Amaro, 2001. Transmission to eels, portals of entry, and putative reservoirs of Vibrio vulnificus E (Biotype 2). Appl. Environ. Microbiol., 67: 4717–4725.

Maule, A. G., R. A. Tripp, Kaattari, and C. B. Schreck, 1989. Stress alters immune function and disease resistance in Chinook salmon (Oncorhynchus tshawytscha). J. Endocrinol., 120: 135–142.

Mazoy, R., R. F. Conchas, B. Fouz, and M. L. Lemos, 1992. Growth of V. anguillarum in different fish sera. Aquaculture, 107: 277–281.

Mesa, M. G., T. P. Poe, A. G. Maule, and C. B. Schreck, 1998. Vulnerability to predation and physiological stress responses in juvenile chinook salmon (Oncorhynchus tshawytscha) experimentally infected with Renibacterium salmoninarum. Can. J. Fish. Aquat. Sci., 55: 1599–1606.

Morvan, C. Le, D. Troutaud, and P. Deschaus, 1998. Differential effects of temperature on specific and nonspecific immune defenses in fish. J. Exp. Biol., 201: 165–168.

Morvan, C. Le, P. Clerton, P. Deschaux, and D. Troutaud, 1997. Effects of environmental temperature on macrophage activities in carp. Fish Shellfish Immunol., 7: 209–212.

Moyner, K., 1993. Changes in serum protein composition occur in Atlantic salmon, Salmo salar L., during Aeromonas salmonicida infection. J. Fish Dis., 16: 601–604.

Muiswinkel, W. B. V., 1992. Fish immunology and fish health. Neth. J. Zool., 42: 494–499.

Muiswinkel, W. B. V., G. F. Wiegertjes, and R. J. M. Stet, 1999. The influence of environmental and genetic factors on the disease resistance of fish. Aquaculture, 172: 103–110.

Muroga, K., and De la Cruz, M. C., 1987. Fate and location of Vibrio anguillarum in tissues of artificially infected ayu (Plecoglossus altivelis). Fish Pathol., 22: 99–103.

Nagae, M., H. Fuda, K. Ura, H. Kawamura, S. Adachi, et al., 1994. The effects of cortisol administration on blood plasma immunoglobulin M (IgM) concentrations in masu salmon (Oncorhynchus masou). Fish Physiol. Biochem., 13: 41–48.

Narnaware, Y. K., and N. Y. S. Woo, 1999. Nuroendocrine regulation of immune function in fish. In: Neural Regulation in the Vertebrate Endocrine System. Prasada Rao, and Peter, eds., Kuwer Academic/Plenum Publishers, New York, pp. 219–231.

Nordmo, R., S. Sevatdal, and A. Ramstad, 1997. Experimental infection with Vibrio salmonicida in Atlantic salmon (Salmo salar L.): an evaluation of three different challenge methods. Aquaculture, 158: 23–32.

Olesen, N. J., and P. E. V. Jorgensen, 1986. Quantification of serum immunoglobulin in rainbow trout Salmo gairdneri under various environmental conditions. Dis. Aquat. Org., 1: 183–189.

Ong, B., 1988. Characteristics of bacteria isolated from diseased groupers, Epinephelus salmonides. Aquaculture, 73: 7–17.

Otto, B. R., A. M. J. J. Verweij-van, and D. M. MacLaren, 1992. Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit. Rev. Microbiol., 18: 217–233.

Pathiratne, A., and W. Rajapakshe, 1998. Hematological changes associated with epizootic ulcerative syndrome in the Asian cichild fish, Etroplus suratensis. Asian Fish. Sci., 11: 203–211.

Pottinger, T. G., and T. R. Carrick, 1999. A comparison of plasma glucose and plasma cortisol as selection markers for high and low stress-responsiveness in female rainbow trout. Aquaculture, 175: 351–363.

Qin, Q., and Pan, J., 1996, Safety and efficacy of Vibrio vulnificus bacterins vaccinated by injection administration against vibriosis in Epinephelus awoara. Trop. Oceanol., 15: 7–12 (in Chinese).

Ransom, D. P., C. N. Lannan, J. S. Rohovec, and J. L. Fryer, 1984. Comparison of histopathology caused by Vibrio anguillarum and Vibrio ordalii in three species of Pacific salmon. J. Fish Dis., 7: 107–115.

Rasheed, V., 1989. Vibriosis outbreak among cultured seabream (Acanthopagrus cuvieri) broodstock in Kuwait. Aquaculture, 76: 189–197.

Rodgers, L. J., and J. B. Burke, 1988. Aetiology of ‘red spot’ disease (vibriosis) with special reference to the ectoparasitic digenean Prototransversotrema streeri (Angel) and the sea mullet, Mugil cephalus L. J. Fish Biol., 32: 655–663.

Saeed, M. O., 1995. Association of Vibrio harveyi with mortalities in cultured marine fish in Kuwait. Aquaculture, 136: 21–29.

Saitanu, K., A. Chongthaleong, M. Endo, T. Umeda, K. Takami, et al., 1994. Antimicrobial susceptibilities and detection of transferable R-plasmids from Aeromonas hydrophila in Thailan. Asian Fish. Sci., 7: 41–46.

Sakai, M., M. Konishi, S. Atsuta, and M. Kobayashi, 1991. The chemiluminescent response of leukocytes from anterior kidney of rainbow trout Oncorhynchus mykiss vaccinated with Vibrio anguillarum, Streptococcus sp. or Renibacterium salmoninarum. Nippon Suisan Gakkaishi. 57: 237–241.

Sakata, T., M. Matsuura, and Y. Shimokawa, 1989. Characteristics of Vibrio damsela isolated from diseased yellowtail, Seriola quinqueradiata. Nippon Suisan Gaikkaishi, 55: 135–141.

Salte, R., K. A. Rorvik, and E. Reed, 1994. Winter ulcers of the skin in Atlantic salmon, Salmo salar L.: Pathogenesis and possible aetiology. J. Fish Dis., 17: 661–665.

Santos, Y., I. Bandin, T. P. Nieto, J. L. Barja, A. E. Toranzo, et al., 1991. Cell-surface associated properties of fish pathogenic bacteria. J. Aquat. Anim. Health, 3: 297–301.

Scapigliati, G., N. Romano, and L. Abelli, 1999. Monoclonal antibodies in fish immunology: identification, ontogeny and activity of T- and B-lymphocytes. Aquaculture, 172: 3–28.

Secombes, C. J., and T. C. Fletcher, 1992. The role of phagocytes in the protective mechanisms of fish. Ann. Rev. Fish Dis., 2: 53–71.

Snieszko, S. F., 1974. The effects of environmental stress on outbreaks of infectious diseases of fishes. J. Fish Biol., 6: 197–208.

Soffientino, B., T. Gwaltney, D. R. Nelson, J. C. Specker, M. Maul, et al., 1999. Infectious necrotizing enteritis and mortality caused by Vibrio carchariae in summer flounder (Paralichthys dentatus) during intensive culture. Dis. Aquat. Org., 38: 201–210.

Spanggaard, B., I. Huber, T. Nielsen, and L. Gram, 2000. Proliferation and location of Vibrio anguillarum during infection of rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis., 23: 423–427.

Svendsen, Y. S., and J. Bogwald, 1997. Influence of artificial wound and non-intact mucus layer on mortality of Atlantic salmon (Salmo salar L) following a bath challenge with Vibrio anguillarum and Aeromonas salmonicida. Fish Shellfish Immunol., 7: 317–325.

Takashahi, Y., T. Kajiwaki, T. Itami, and T. Okamoto, 1987. Enzymatic properties of the bacteriolytic substances in the skin mucus of yellowtail. Bull. Jap. Soc. Sci. Fish., 53: 426–431.

Thune, R. L., L. A. Stanley, and R. K. Cooper, 1993. Pathogenesis of Gram-negative bacterial infections in warm-water fish. Ann. Rev. Fish Dis., 37–68.

Tiainen, T., J. L. Larsen, and S. Pelkonen, 1994. Characterization of Vibrio anguillarum strains isolated from diseased fish in Finland. Acta Vet. Scand., 35: 355–362.

Tison, D. L., M. Nishibuchi, J. D. Greenwood, and R. J. Seidler, 1982. Vibrio vulnificus biotype 2: a new biotype pathogenic for eels. Appl. Environ. Microbiol., 44: 640–646.

Tolmasky, M. E., and J. H. Crosa, 1984. Molecular cloning and expression of genetic determinants for the iron uptake system mediated by the Vibrio anguillarum plasmid pJM1. J. Bacteriol., 160: 860–866.

Tolmasky, M. E., L. A. Actis, A. E. Toranzo, J. L. Barja, and J. H. Crosa, 1985. Plasmid mediated from uptake in Vibrio anguillarum strains isolated from turbot in Spain. J. Gen. Microbiol., 131: 1989–1997.

Toranzo, A. E., and J. L. Barja, 1993. Virulence factors of bacterial pathogenic for coldwater fish. Ann. Rev. Fish Dis., 3: 5–36.

Toranzo, A. E., J. L. Barja, and F. M. Hetrick, 1982. Survival of Vibrio anguillarum and Pasteurella piscicida in estuarine and fresh waters. Bull. Eur. Assoc. Fish Pathol., 3: 43–45.

Toranzo, A. E., J. L. Barja, R. R. Colwell, F. M. Hetrick, and J. H. Crosa, 1983. Hemagglutinating, hemolytic and cytotoxic activities of Vibrio anguillarum and related vibrios isolated from stripped bass on the Atlantic coast. FEMS Microbiol., 18: 257–262.

Toranzo, A. E., Y. Santos, M. L. Lemos, A. Ledo, and J. Bolinches, 1987. Homology of Vibrio anguillarum strains causing epizootics in turbot, salmon and trout reared on the Atlantic coast of Spain. Aquaculture, 67: 41–52.

Totland, G. K., and A. Nylund, 1988. An ultrastructural study of morphological changes in Atlantic salmon, Salmo salar L., during the development of cold water vibriosis. J. Fish Dis., 11: 1–13.

Vera, P., J. I. Navas, and B. Fouz, 1991. First isolation of Vibrio damsela from seabream (Sparus aurata). Bull. Eur. Ass. Fish Pathol., 11: 112–113.

Villamil, L., A. Figueras, A. E. Toranzo, M. Pianas, and B. Novoa, 2003a. Isolation of a highly pathogenic Vibrio pelagius strain associated with mass mortalities of turbot, Scophthalmus maximus (L.), larvae. J. Fish Dis., 26: 293–303.

Villamil, L., A. Figueras, R. Aranguren, and B. Novoa, 2003b. Non-specific immune response of turbot, Scophthalmus maximus (L.) experimentally infected with a pahtogenic Vibrio pelagius. J. Fish Dis., 26: 321–329.

Wang, R., and M. Belosevic, 1994. Estradiol increases susceptibility of goldfish to Trypanosoma danilewski. Dev. Comp. Immunol., 18: 377–387.

Wang, X. H., and K. Y. Leung, 2000. Biochemical characterization of different types of adherence of Vibrio species to fish epithelial cells. Microbiology, 146: 989–998.

Wang, X. H., H. L. Oon, G. W. P. Ho, W. S. F. Wong, T. M. Lim, et al., 1998. Internalization and cytotoxicity are important virulence mechanisms in vibrio-fish epithelial cell interactions. Microbiology, 144: 2987–3002.

Wiik, R., K. Anderson, I. Uglenes, and E. Egidius, 1989. Cortisol-induced increase in susceptibility of Atlantic salmon, Salmo salar, to Vibrio salmonicida, together with effects on the blood cell pattern. Aquaculture, 83: 201–215.

Wolf, M. K., and J. H. Crosa, 1986. Evidence for the role of a siderophore in promoting Vibrio anguillarum infections. J. Gen. Microbiol., 132: 2949–2952.

Woo, N. Y. S., J. Li, and E. E. Deane, 2001. Potential use of vaccines against vibriosis in sea bream. Aquaculture, 2001, Orlando, Florida, U.S.A., pp. 698.

Woo, N. Y. S., J. L. M. Ling, and K. M. Lo, 1995. Pathogenic Vibrio spp. in the sea bream, Sparus sarba. J. Sun Yatsen Univ. (Supplement), 3: 192–193.

Wu, H., and Pan, J., 1997. studies on the pathogenic bacteria of the vibriosis of Seriola dumerili in marine cage culture. J. Fish China, 21: 171–174 (in Chinese).

Wu, H., and Pan, J., 2000. Experimental studies of the effects of vaccination against vibriosis in marine-cage cultured red seabream (Pagrus major). In: Proceedings of International Symposium on Marine Biotechnology. Xu, H. S., ed., China Ocean Press, Beijing, pp. 359–364.

Xiao, H., Li, J., Wang, X. H., Ji, W. S., and Xu, H. S., 1999. Studies on pathogens of rotted gills and caudal fins of sea perch (Lateolabrax japonicus). J. Ocean Univ. Qingdao, 29: 87–93.

Zapata, A. G., A. Chiba, and A. Varas, 1996. Cells and tissues of the immune system of fish. In: The Fish Immune System: Organism, Pathogen, and Environment. G. K. Iwama, and Nakanishi, T., eds., Academic Press, London, pp. 1–53.

Zhang, X. H., and B. Austin, 2000. Pathogenicity of Vibrio harveyi to salmonids. J. Fish Dis., 23: 93–102.

Zhang, X. H., P. G. Meaden, and B. Austin, 2001. Duplication of hemolysin genes in a virulent isolate of Vibrio haveyi. Appl. Environ. Microbiol., 67: 3161–3167.

Zhu, C. H., He, J. G., and Huang, Z. J., 2000. Identification and pathogenicity of pathogen of E. awoara and Epinephalus fario ulceration disease. Acta Scientiarum Naturalium Universitatis Sunyatseni (Supplement), 39: 278–282 (in Chinese).

Zorrilla, I., S. Arijo, M. Chabrillon, P. Diaz, E. Martinez-Manzanares, 2003. Vibrio species isolated from diseased farmed sole, Solea senegelensis (Kaup), and evaulation of the potential virulence role of their extracellular products. J. Fish Dis., 26: 103–108.