epizootic haematopoietic necrosis

Identity

Preferred Scientific Name

• epizootic haematopoietic necrosis

International Common Names

• English: epizootic hematopoietic necrosis; iridovirus of catfish disease; sheatfish iridovirus disease; systemic iridovirus diseases caused by ranaviruses

English acronym

• EHN

Pathogen/s

Overview

Epizootic haematopoietic necrosis (EHN) is a systemic iridovirus (Ranavirus) infection of redfin perch (Perca fluviatilis), rainbow trout (Oncorhynchus mykiss), sheatfish (Silurus glanis) and catfish (Ictalurus melas) (Ahne et al., 1989; Aubertin, 1991; Langdon et al., 1986; Pozet et al., 1992). The disease is caused by three similar viruses: epizootic haematopoietic necrosis virus (EHNV), European sheatfish virus (ESV) and European catfish virus (ECV) (Ahne et al., 1989; Hedrick et al., 1992; Langdon, 1989; Pozet et al., 1992; Reddacliff and Whittington, 1996). The geographical range of EHNV is currently restricted to Australia (Hyatt et al., 2000; Wolf, 1988). The ECV and ESV agents have only been detected among fish in Europe (Ahne et al., 1998; Ahne et al., 1989; Pozet et al., 1992). Although inducing similar diseases in their respective hosts, EHNV, ECV and ESV are distinct agents distinguished by molecular techniques (Hyatt et al., 2000; Mao et al., 1997; Tapiovaara et al., 1998).

EHN infection in redfin perch is generally lethal (Whittington et al., 1995). Rainbow trout are relatively resistant and only a small proportion of individuals become infected (Whittington et al., 1994; Whittington and Reddacliff, 1995; Whittington et al., 1999). Infections with ESV and ECV can induce high morbidity and mortality in their catfish hosts (Ahne et al., 1989, Pozet et al., 1992). The disease caused by all three iridoviruses is characterised by mortalities due to necrosis in the liver, spleen, haematopoietic tissue of the kidney and other tissues. Experimental exposure studies have shown that rainbow trout can be infected with ECV and ESV without showing morbidity and mortality (Ahne et al., 1998).

Iridoviridae of the genus ranavirus are becoming increasingly important as pathogens of feral, cultured and ornamental teleosts. They are endotheliotropic and can induce severe disease in susceptible fish species, characterized by necrotic lesions in vascular walls and visceral organs. The group consists of the epizootic haematopoietic necrosis virus (EHNV) (Langdon et al., 1986b; Eaton et al., 1991; Hedrick et al., 1992), isolates from two ictalurid fishes in Europe (Ahne et al., 1989; Pozet et al., 1992), turbot (Scophthalmus maximus) iridovirus-like agent (Bloch and Larsen, 1993), an isolate from two freshwater tropical ornamental species (Hedrick and McDowell, 1995) and largemouth bass virus (LMBV) (Plumb et al., 1996). The present discussion considers mainly diseases caused by EHNV and ictalurid viruses, which can cause 100% mortality in young susceptible warm-water hosts. The economic damage is rare but serious.

The type strain of ranavirus is the frog virus 3 (FV3) (Granoff et al., 1965; Essani and Granoff, 1989; Aubertin, 1991). Hedrick et al. (1992) suggested that EHNV and ictalurid isolates were strains of FV3. The amphibian group in ranavirus genus includes amphibian viruses from North America (Essani and Granoff, 1989), the European green frog virus (Fijan, 1999; Ahne et al., 1995) and the Australian Bohle (or burrowing frog) iridovirus (Speare and Smith, 1992; Hengstberger et al., 1993). The North American tadpole oedemavirus and the European frog virus are not pathogenic for fish tested in experiments (Wolf et al., 1968; Fijan, 1999), but the Bohle iridovirus induced 100% mortality in bath infected barramundi (Lates calcarifer) (Moody and Owens, 1994). The latter report indicates the possible importance of amphibian ranaviruses for finfish aquaculture.

Epizootic haematopoietic necrosis and EHNV were reviewed by Wolf (1988) and McAllister (1993a). This datasheet describes EHN in redfin perch.

Topics for Further Studies

The development of methods for distinguishing ranavirus isolates requires further attention. Such methods are needed to study epizootiology and taxonomy. Surveys of sheatfish, bullhead, ornamental and other fish production sites for ranaviruses in fish and amphibians are needed to assess the range, extent and significance of currently known and possible other diseases in this group. Studies on host ranges and reciprocal pathogenicity of fish and amphibian ranaviruses for early life stages could help to detect virus sources and reservoirs.

[Based upon material originally published in Woo PTK, Bruno DW, eds., 1999. Fish diseases and disorders, Vol. 3 Viral, bacterial and fungal infections. Wallingford, UK: CABI Publishing.]

Host Animals

Hosts/Species Affected

Members of the ranavirus genus were isolated from freshwater fishes on three continents. Epizootic haemopoietic necrosis virus affects redfin perch (Percafluviatilis) and rainbow trout (Langdon et al., 1986a, b, 1988; Langdon and Humphrey, 1987) in Australia (Victoria, New South Wales, and South Australia).Sheatfish iridovirus (or IW for iridovirus wels) was isolated in Germany (Ahne et al., 1989). Black bullhead iridovirus (or ICF for iridovirus of catfish) caused mortality of Ameiurus melas (syn. Ictalurus melas) in France (Pozet et al., 1992) and in Italy (Bovo et al., 1993). Iridovirus of ornamental tropical fish (IOTF) was isolated from imported guppy (Poecilia reticulata) and doctor fish (Labroides dimidatus) in California, USA (Hedrick and McDowell, 1995).Largemouth bass virus was isolated from a mortality among adult largemouth bass in a reservoir in South Carolina, USA (Plumb et al., 1996).

The redfin perch and rainbow trout isolates of EHNV are serologically indistinguishable. Langdon (1989) experimentally infected 11 teleosts. The mosquito fish (Gambusia affinis) is the only species besides redfin perch which is susceptible to horizontal transmission. Four native species are highly susceptible to the virus and at least one of them (Macquarie perch, Macquaria australasia) is in decline. Atlantic salmon (Salmo salar) develops clinical disease but the infection is not lethal. Barramundi is refractory and so are two exotic cyprinids, which do not seem to be the original host (Langdon, 1989). Whittington et al. (1996) demonstrated the spread of EHN in redfin perch to river systems and impoundments in Australia. In outbreaks of sheatfish and black bullhead diseases (Ahne et al., 1989; Pozet et al., 1992), the water environment contained several other warm-water species, including cyprinids, pike and perch, but they remained unaffected. The ornamental fish strain is pathogenic for rainbow trout (Hedrick and McDowell,1995). Largemouth bass virus has not induced mortality in infected adult largemouth bass (Plumb et al., 1996).

The factors modulating the susceptibility of fish to EHNV, ESV and ECV infection are poorly understood. Clinical outbreaks due to EHNV are associated with poor water quality. In rainbow trout, infection occurs naturally at water temperatures from 11 to 17°C and experimentally from 8 to 21°C (Whittington et al., 1994). Disease in redfin perch does not occur at temperatures below 12°C. The following fish species were found to be susceptible to EHNV following bath exposure: redfin perch, rainbow trout, Macquarie perch (Macquaria australasica), mosquito fish (Gambusia affinis), silver perch (Bidyanus bidyanus) and mountain galaxias (Galaxias olidus) (Langdon, 1989). Both juvenile and adult redfin perch may be affected in outbreaks, but juveniles may be more susceptible to the disease. EHNV has now been detected in diseased rainbow trout ranging from hatchery fry to table-sized fish, although mortalities are most often seen in 0+ fish up to 125 mm fork-length.

Distribution

The reported geographical ranges of fish ranaviruses are so far restricted to respective continents of isolation. However, that from exotic ornamental fish is suspected to be a part of putative transcontinental transmission (Hedrick and McDowell, 1995). The Bohle iridovirus, which is present only in Queensland, is geographically distinct from EHNV (Speare and Smith, 1992).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Pathology

EHN

Focal necrosis is a consistent finding in haematopoietic kidney and liver of naturally and experimentally infected fish. In the spleen and pancreas, this sign is variable. Necrotic haemopoietic cells are disseminated in all vessels. Lesions in other susceptible species are inconstant (Langdon, 1989). The most consistent is the necrosis in haemopoietic kidney and liver. A description of gross lesions in redfin perch by Reddacliff and Whittington (1996) includes haemorrhage around bases of fins, focal haemorrhage in gills, oedema and multiple necrotic foci in liver. Microscopic changes consist of focal to extensive necrosis in haematopoietic kidney, liver, spleen, heart, pancreas and lamina propria of the intestine. Thrombosis, haemorrhage and fibrinous exudate are common in gills. Lesions in rainbow trout are similar but milder.

Sheatfish Iridovirus Disease

Histopathology and electron microscopy in experimentally infected sheatfish of 4-5 cm revealed alterations in all organs (Ogawa et al., 1990). Endothelium and reticuloendothelial cells are the main target. Periarteriolar necrosis of the haemopoietic tissue and degeneration of tubular and duct epithelia are prominent in kidneys. Gill epithelium and chloride cells are hyperplastic and oedematous. The lumen of the circulatory system is congested and the proliferating cells contain eosinophilic inclusions. Alterations in the skin include proliferation and necrosis of epithelial cells, hyperplasia of monocellular glands and zonal haemorrhage in hypodermis. Myocarditis and endocarditis are diffuse. Small necrotic foci are seen in the liver and spleen. Glial proliferation and spongiosis in the brain are also pronounced. The pathology and incubation most closely resemble those of EHN.

Iridovirus of Catfish Disease

The kidney is the principal target organ and both the haematopoietic and the excretory part are severely altered. Blood vessel walls are damaged. Necroses in the spleen and kidney can be severe. Interlamellar spaces in gills are obliterated and lamellar fusion is evident (Pozet et al., 1992).

Diagnosis

Fish ranaviruses are endotheliotropic and cause haemorrhagic diathesis, oedema and peripheral circulatory failure.

EHN

Epizootic haematopoietic necrosis appeared during the spring of 1984 in a lake and caused severe mortality among juvenile redfin perch. The disease is less serious in farmed rainbow trout. Experimentally infected 35-45-day-old redfin perch develop depression, skin darkening and erratic swimming and die after 4-5 days (Langdon, 1989). Some have erythema around the brain and nostrils. Clinical signs in disease outbreaks described by Langdon and Humphrey (1987) are identical, except for skin ulcers invaded by fungus in some fish.

Sheatfish Iridovirus Disease

The sheatfish iridovirus disease (iridovirous wels disease (IWD)) is characterized by loss of appetite, apathy, ataxia (including rapid spiral swimming), petechial haemorrhage in skin and internal organs and generalized destruction of haematopoietic tissues in the kidney and spleen. The cumulative fry mortality in a recirculation system was 100% (Ahne et al., 1989). Fry infected by bath in virus suspension and by cohabitation also succumbed to high mortality within 8 and 11 days, respectively (Ahne et al., 1990). Adult fish are also susceptible but mortality does not exceed 30% (Ahne et al., 1991).

Iridovirus of Catfish Disease

Iridovirus of ornamental tropical fish was isolated from carriers but the experimental infection of rainbow trout induced low mortality, considerable lesions in the kidney and spleen and virus titres greater than 10⁸ TCID₅₀ g^-1 (Hedrick and McDowell, 1995).

Experimental infection of barramundi with Bohle iridovirus resulted in mortality and focal necrosis in the liver (Moody and Owens, 1994).

Procedures recommended by the OIE Manual (1995b) for EHNV are applicable to other viruses in the ranavirus group considered in this chapter. Presumptive diagnosis is based on clinical signs, virus isolation in BF-2 or other susceptible cells and electron microscopy. Identification of EHNV is based on IFAT or ELISA tests (OIE Manual, 1995b) and PCR (Gould et al., 1995). Other viruses in the group show antigenic relatedness to EHNV and FV3 demonstrable by IFAT (Hedrick et al., 1992; Ahne et al., 1995; Hedrick and McDowell, 1995), Western blotting and nucleic acid hybridization (Hedrick and McDowell, 1995).

Epizootic haematopoietic necrosis virus is detectable by ELISA, immunohistochemistry and electron microscopy (Hyatt et al., 1991). An improved antigen-capture ELISA (Whittington and Steiner, 1993) can recognize EHNV in clarified fish tissue and in cell-culture supernatant. The lowest detectable level of the virus in supernatant is 103.5 TCID50 ml^-1. Sensitivity and specificity of this method for tissue samples are about 81 and 99%, respectively, and for cellculture supernatant 96 and close to 100%. Manual grinding with a pestle in a tube, followed by vortexing in the same tube with 3 mm glass beads and clarification in a microcentrifuge, is the most efficient method for releasing EHNV from tissue samples (Whittington and Steiner, 1993).

The viruses do not induce differentiating neutralising antibodies in mammals or fish (Hyatt et al., 2000). The viruses can be identified by immunofluorescence, enzyme-linked immunosorbent assays (ELISAs) or immunoelectron microscopy (Hedrick et al., 1992; Hengstberger et al., 1993; Hyatt et al., 1991; Hyatt et al., 2000; Steiner et al., 1991). EHNV has several antigens in common with ESV and ECV from Europe and at least one antigen in common with the amphibian iridoviruses from North America (frog virus 3) and Australia (Bohle iridovirus) (Ahne et al., 1995; Hedrick et al., 1992; Hengstberger et al., 1993). Antigen-detection tests with polyclonal antibodies against EHNV detect each of these viruses. Sodium dodecyl sulphate-polyacrylamide gel electrophoresis (SDS-PAGE), Western blotting and polymerase chain reaction (PCR) can differentiate to varying degrees between the different viruses (Hyatt et al., 2000; Mao et al., 1997).

The screening and diagnostic procedures for EHNV, ESV and ECV are based on isolation of virus in cell culture, ELISA, indirect fluorescent antibody tests (IFAT), and electron microscopy (Ahne et al., 1989; Eaton et al., 1991; Hedrick et al., 1992; Hyatt et al., 1991; Langdon et al., 1986; Pozet et al., 1992; Steiner et al., 1991). Antigen-capture ELISA has a sensitivity of 60-80% depending on the stage of infection when used to test tissues from both rainbow trout and redfin perch (Hyatt et al., 1991; Steiner et al., 1991; Whittington et al., 1995; Whittington and Steiner, 1993). Antigen-capture ELISA is the method of choice for confirming the cause of cytopathic effect in cell culture; IFAT and electron microscopy are also useful. IFAT or immunoperoxidase staining may also be used for diagnosis on formalin-fixed tissues. PCR may be used to detect Ranavirus DNA in infected tissues (6). Western blots, SDS-PAGE and PCR sequencing can be used to specifically identify EHNV, ESV and ECV (Hyatt et al., 2000; Mao et al., 1997).

The diagnosis of epizootic haematopoietic necrosis (EHN) is based on direct methods that are either the isolation of virus (epizootic haematopoietic necrosis virus [EHNV], European sheatfish virus [ESV] and European catfish virus [ECV]) in cell culture followed by its immunological identification (conventional approach), or the immunological demonstration of virus antigen in infected fish tissues.

Due to insufficient knowledge of the serological responses of fish to virus infections, the detection of fish antibodies to viruses has not thus far been recognised as a valuable diagnostic method for assessing the virus status of fish populations. In the case of EHNV, preliminary investigations using enzyme-linked immunosorbent assay (ELISA) in known infected rainbow trout populations have revealed up to 1% prevalence of seropositive fish in adult age classes. Further investigation of the epidemiology of EHNV in rainbow trout is needed before serological results can be interpreted.

List of Symptoms/Signs

Disease Course

Adult redfin perch is extremely susceptible to EHNV infection by bath and i.p. inoculation. As little as 0.08 TCID50 ml^-1 was lethal at 19-21°C. The incubation period at this temperature is 11 days and at 13-19°C up to 28 days. Disease does not develop below 12°C (Whittington and Reddacliff, 1996). Virus replication in endothelial cells results in necrosis and consequent haemorrhage.

The immunological response in fish and rabbits does not generally include neutralizing antibodies. One survivor of ICFD had neutralizing antibodies (Pozet et al., 1992). However, rabbits react to these viruses by producing antibodies suitable for IFAT and ELISA. Redfin perch survivors from natural disease outbreaks are resistant to challenge with EHNV (Langdon, 1989). The epizootiology of EHN in rainbow trout suggests that this species is incapable of developing long-lasting resistance (OIE Manual, 1995b).

Epidemiology

The epidemiology of EHNV in rainbow trout is incompletely understood (Whittington et al., 1994; Whittington and Reddacliff, 1995; Whittington et al., 1999). Due to their extreme susceptibility, it is unlikely that redfin perch are a natural host (Whittington and Hyatt, 1996; Whittington et al., 1995). Infection may recur annually at a rainbow trout production site and this may be due to reinfection from wild redfin perch in the catchment area. A carrier state in naturally infected rainbow trout appears to be very uncommon as neither EHNV antigen nor anti-EHNV antibody are routinely detected in rainbow trout surviving an outbreak (Whittington et al., 1980; Whittington et al., 1999). However, the disease can occur at a very low frequency in an infected population, and mortalities may not exceed the usual background rate. Thus infected fish could easily be included in batches of healthy translocated fish and there is good evidence that this has occurred. No epidemiological data are available for ESV or ECV.

Natural epizootics of EHN in early summer among young redfin perch last for 2-3 weeks. They are recurrent in several major waterways in Victoria, Australia (Langdon, 1989). Adults are rarely affected. Virus isolation from juveniles and adults immediately after an epizootic is infrequent (Langdon and Humphrey, 1987). 100-day-old survivors of disease outbreaks are resistant to challenge (Langdon, 1989). Redfin perch carriers were not detected and there is no evidence for vertical transmission. An unknown reservoir and carrier host are suspected. Silver gulls (Larus novaehollandiae) and great cormorants (Phalacrocorax carbo) can spread EHNV by the regurgitation of ingested material (Whittington et al., 1996). Other means of spread include transportation of fish by humans, transfer on boats, nets and other equipment as well as water flow and migration of carrier fish in a catchment area (Whittington et al., 1996). The epizootiology of other diseases in the group was not studied.

The close relatedness of fish and amphibian ranaviruses and the pathogenicity of Bohle iridovirus for barramundi should be kept in mind in programmes for avoidance of pathogens in aquaculture (Hedrick et al., 1992; Ahne et al., 1995). Frogs are ubiquitous on large farms for warm-water fishes. These could be reservoirs and vectors of fish pathogens. Hedrick et al. (1992), Hedrick and McDowell (1995) and Hedrick (1996) consider transcontinental movements of amphibians and exotic ornamental fish as possible reasons for the appearance of similar viruses in Australia and Europe. It was suggested that control be extended to aquatic amphibians and tropical aquarium fishes (Ahne et al., 1995; Hedrick, 1996).

Impact Summary

Zoonoses and Food Safety

This species is not a zoonosis.

References

Ahne W, Bearzotti M, Bremont M, Essbauer S, 1998. Comparison of European systemic piscine and amphibian iridoviruses with epizootic haematopoietic necrosis virus and frog virus 3. Journal of Veterinary Medicine. Series B, 45(6):373-383

Ahne W, Matasin Z, Bovo G, 1995. Antigenic relationship of epizootic haematopoietic necrosis virus (EHNV) and iridovirus-like isolates from European green frogs (Rana esculenta). Bulletin of the European Association of Fish Pathologists, 15(4):142-144

Ahne W, Ogawa M, Schlotfeldt HJ, 1990. Fish viruses: transmission and pathogenicity of an icosahedral cytoplasmic deoxyribovirus isolated from sheatfish (Silurus glanis). Journal of Veterinary Medicine. Series B, 37(3):187-190

Ahne W, Schlotfeldt HJ, Thomsen I, 1989. Fish viruses: isolation of an icosahedral cytoplasmic deoxyribovirus from sheatfish (Silurus glanis). Journal of Veterinary Medicine, B (Infectious Diseases, Immunology, Food Hygiene, Veterinary Public Health), 36(5):333-336

Anhe W, Schlotfeldt HJ, Ogawa M, 1991. Iridovirus infection of adult sheatfish (Silurus glanis). Bulletin of the European Association of Fish Pathologists, 11(3):97-98

Aubertin AM, 1991. Family Iridoviridae. In: Francki RIB, Fauquet CM, Knudson DL, Brown F, eds. Classification and Nomenclature of Viruses. Fifth Report of the International Committee on Taxonomy of Viruses. Archives of Virology, Suppl. 2, 132-136

Berry ES, Shea TB, Gabliks J, 1983. Two iridovirus isolates from Carassius auratus (L.). Journal of Fish Diseases, 6(6):501-510

Bloch B, Larsen JL, 1993. An iridovirus-like agent associated with systemic infection in cultured turbot Scophthalmus maximus fry in Denmark. Diseases of Aquatic Organisms, 15(3):235-240

Bovo G, Comuzi M, DeMas S, Ceshia G, Giorgetti G, Giacometti P, Capellozza E, 1993. Isolamento di un agente virale Irido-like da pesce gatto (Ictalurus melas) d,allevamento. Bolletino della Società Italiana di Patologia Ittica 11:3-10

Doyle KA, Beers PT, Wilson DW, 1996. Quarantine of aquatic animals in Australia. Revue Scientifique et Technique - Office International des Épizooties, 15(2):659-673

Eaton BT, Hyatt AD, Hengstberger S, 1991. Epizootic haematopoietic necrosis virus: purification and classification. Journal of Fish Diseases, 14(2):157-169

Essani K, Granoff A, 1989. Properties of amphibian and piscine iridoviruses: a comparison. In: Ahne W, Kurstak E, eds. Viruses of Lower Vertebrates. Berlin: Springer-Verlag, 79-85

Fijan, N., 1999. Spring viraemia of carp and other viral diseases and agents of warm-water fish. In: Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections, [ed. by Woo, P. T. K., Bruno, D. W.]. Wallingford, UK: CAB International. 177-244.

Gould AR, Hyatt AD, Hengstberger SH, Whittington RJ, Coupar BEH, 1995. A polymerase chain reaction (PCR) to detect epizootic haematopoietic necrosis virus and Bohle iridovirus. Diseases of Aquatic Organisms, 22(3):211-215

Granoff A, Came PE, Rafferty KA, 1965. The isolation and properties of viruses from Rana pipiens: their possible relationship to renal adenocarcinoma of the leopard frog. Annals of the New York Academy of Sciences, 126:237-255

Granzow H, Wieland F, Fichtner, D, Enzmann PJ, 1997. Studies on the ultrastructure and morphogenesis of fish pathogenic viruses grown in cell culture. Journal of Fish Diseases, 20:1-10

Hedrick RP, 1996. Movements of pathogens with the international trade of live fish: problems and solutions. Revue Scientifique et Technique - Office International des Épizooties, 15(2):523-531

Hedrick RP, McDowell TS, 1995. Properties of iridoviruses from ornamental fish. Veterinary Research, 26(5/6):423-427

Hedrick RP, McDowell TS, Ahne W, Torhy C, Kinkelin Pde, 1992. Properties of three iridovirus-like agents associated with systemic infections of fish. Diseases of Aquatic Organisms, 13(3):203-209

Hengstberger SG, Hyatt AD, Speare R, Coupar BEH, 1993. Comparison of epizootic haematopoietic necrosis and Bohle iridoviruses, recently isolated Australian iridoviruses. Diseases of Aquatic Organisms, 15(2):93-107

Hyatt AD, Eaton BT, Hengstberger S, Russel G, 1991. Epizootic necrosis virus: detection by ELISA, immunohistochemistry and immunoelectron-microscopy. Journal of Fish Diseases, 14(6):605-617

Hyatt AD, Gould AR, Zupanovic Z, Cunningham AA, Hengstberger S, Whittington RJ, Kattenbelt J, Coupar BEH, 2000. Comparative studies of piscine and amphibian iridoviruses. Archives of Virology, 145(2):301-331

Langdon JS, 1989. Experimental transmission and pathogenicity of epizootic haematopoietic necrosis virus (EHNV) in redfin perch, Perca fluviatilis L., and 11 other teleosts. Journal of Fish Diseases, 12(4):295-310

Langdon JS, Humphrey JD, 1987. Epizootic haematopoietic necrosis, a new viral disease in redfin perch, Perca fluviatilis L., in Australia. Journal of Fish Diseases, 10(4):289-297

Langdon JS, Humphrey JD, Copland J, Carolane R, Gudkovs N, Lancaster C, 1986. The disease status of Australian salmonids: viruses and viral diseases. Journal of Fish Diseases, 9(2):129-135

Langdon JS, Humphrey JD, Williams LM, 1988. Outbreaks of an EHNV-like iridovirus in cultured rainbow trout, Salmo gairdneri Richardson, in Australia. Journal of Fish Diseases, 11(1):93-96

Langdon JS, Humphrey JD, Williams LM, Hyatt AD, Westbury HA, 1986. First virus isolation from Australian fish: an iridovirus-like pathogen from redfin perch, Perca fluviatilis L. Journal of Fish Diseases, 9(3):263-268

Mao JingHe, Hedrick RP, Chinchar VG, 1997. Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology (New York), 229(1):212-220

McAllister PE, 1993. Freshwater temperate fish viruses. In: Stoskopf MK, ed. Fish Medicine. Philadelphia: WB Saunders, 284-300

Miocevic I, Smith J, Owens L, Speare R, 1993. Ultraviolet sterilisation of model viruses important to finfish aquaculture in Australia. Australian Veterinary Journal, 70(1):25-27

Moody NJG, Owens L, 1994. Experimental demonstration of the pathogenicity of a frog virus, Bohle iridovirus, for a fish species, barramundi Lates calcarifer. Diseases of Aquatic Organisms, 18(2):95-102

Office International des Épizooties, 1995. Diagnostic manual for aquatic animal diseases. Diagnostic manual for aquatic animal diseases., Ed. 1:xiv + 195 pp

Ogawa M, Ahne W, Fischer-Scherl T, Hoffmann RW, Schlotfeldt HJ, 1990. Pathomorphological alterations in sheatfish fry Silurus glanis experimentally infected with iridovirus-like agent. Diseases of Aquatic Organisms, 9(3):187-191

OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (data set for 2004). Paris, France: Office International des Epizooties

OIE, 2009. World Animal Health Information Database - Version: 1.4. World Animal Health Information Database. Paris, France: World Organisation for Animal Health. http://www.oie.int

Plumb JA, Grizzle JM, Young HE, Noyes AD, Lamprecht S, 1996. An iridovirus isolated from wild largemouth bass. Journal of Aquatic Animal Health, 8(4):265-270

Pozet F, Morand M, Torhy C, de Kinkelin P, 1992. Isolation and preliminary characterization of a pathogenic icosahedral deoxyribovirus from the catfish Ictalurus melas. Diseases of Aquatic Organisms, 14:35-42

Reddacliff LA, Whittington RJ, 1996. Pathology of epizootic haematopoietic necrosis virus (EHNV) infection in rainbow trout (Oncorhynchus mykiss Walbaum) and redfin perch (Perca fluviatilis L.). Journal of Comparative Pathology, 115(2):103-115

Sano, M., Nakai, T., Fijan, N., 2011. Viral diseases and agents of warmwater fish. In: Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections, (Ed. 2) [ed. by Woo, P. T. K., Bruno, D. W.]. Wallingford, UK: CABI. 166-244. http://www.cabi.org/cabebooks/ebook/20113056498 doi: 10.1079/9781845935542.0166

Speare R, Smith JR, 1992. An iridovirus-like agent from the ornate burrowing frog Limnodynastes ornatus in northern Australia. Diseases of Aquatic Organisms, 14:51-57

Steiner KA, Whittington RJ, Peterson RK, Hornitzky C, Garnett H, 1991. Purification of epizootic haematopoietic necrosis virus and its detection using ELISA. Journal of Virological Methods, 33(1, 2):199-209

Tapiovaara H, Olesen NJ, Lindén J, Rimaila-Pärnänen E, Bonsdorff CHvon, 1998. Isolation of an iridovirus from pike-perch Stizostedion lucioperca. Diseases of Aquatic Organisms, 32(3):185-193

Whittington RJ, Hyatt AD, 1996. Contingency planning for control of epizootic haematopoietic necrosis disease. Singapore Veterinary Journal, 20:79-87

Whittington RJ, Kearns C, Hyatt AD, Hengstberger S, Rutzou T, 1996. Spread of epizootic haematopoietic necrosis virus (EHNV) in redfin perch (Perca fluviatilis) in southern Australia. Australian Veterinary Journal, 73(3):112-114

Whittington RJ, Philbey A, Reddacliff GL, Macgown AR, 1994. Epidemiology of epizootic haematopoietic necrosis virus (EHNV) infection in farmed rainbow trout, Oncorhynchus mykiss (Walbaum): findings based on virus isolation, antigen capture ELISA and serology. Journal of Fish Diseases, 17(3):205-218

Whittington RJ, Reddacliff GL, 1995. Influence of environmental temperature on experimental infection of redfin perch (Perca fluviatilis) and rainbow trout (Oncorhynchus mykiss) with epizootic haematopoietic necrosis virus, an Australian iridovirus. Australian Veterinary Journal, 72(11):421-424

Whittington RJ, Reddacliff LA, Marsh I, Kearns C, Zupanovic Z, Callinan RB, 1999. Further observations on the epidemiology and spread of epizootic haematopoietic necrosis virus (EHNV) in farmed rainbow trout Oncorhynchus mykiss in southeastern Australia and a recommended sampling strategy for surveillance. Diseases of Aquatic Organisms, 35(2):125-130

Whittington RJ, Steiner KA, 1993. Epizootic haematopoietic necrosis virus (EHNV): improved ELISA for detection in fish tissues and cell cultures and an efficient method for release of antigen from tissues. Journal of Virological Methods, 43(2):205-220

Wolf K, 1988. Fish viruses and fish viral diseases. Fish viruses and fish viral diseases., xii + 476 pp

Wolf K, Bullock GL, Dunbar CE, Quimby MC, 1968. Tadpole edema virus: a viscerotropic pathogen for anuran amphibians. Journal of Infectious Diseases, 118:253-262

Distribution References

CABI, Undated. Compendium record. Wallingford, UK: CABI

CABI, Undated a. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

OIE Handistatus, 2005. World Animal Health Publication and Handistatus II (dataset for 2004)., Paris, France: Office International des Epizooties.

OIE, 2009. World Animal Health Information Database - Version: 1.4., Paris, France: World Organisation for Animal Health. https://www.oie.int/

Sano M, Nakai T, Fijan N, 2011. Viral diseases and agents of warmwater fish. In: Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections. [ed. by Woo P T K, Bruno D W]. Wallingford, UK: CABI. 166-244. http://www.cabi.org/cabebooks/ebook/20113056498 DOI:10.1079/9781845935542.0166

Distribution Maps