Aquaculture

ELSEVIER Aquaculture 132 ( 1995) 43-52

Viruses and viral diseases of salmonids

Tokuo Sane
Laboratory of Aquatic Pathology, Department of Aquatic Biosciences, Tokyo Vniversiry of Fisheries, 4-5-7 Konan, Minato-ku, Tokyo 108, Japan

Abstract Salmonid fishes are one of the most important aquatic resources in the world, and since salmonid fish culture was initiated many years ago, it has been developing with the times in several countries. In particular, the intensive culture of rainbow trout, Oncorhynchus mykiss, has developed over the past 30 years in the USA, Europe, Japan and elsewhere. However, the successes achieved have brought with them diverse new disease problems for rainbow trout and other salmonids. The crucial problems are communicable or infectious diseases caused by bacterial and viral agents, among which viral disease is the most serious, because diagnosis is difficult, the majority of the epizootics is acute or subacute, and furthermore, no chemotherapy is available for them. The viral agents, the viral infections and the pathologic conditions of salmonid fishes can be grouped into the respective viral families according to the attributes of the virus, and into an unclassified virus group as follows. RNA VIRUS GROUP: Bimaviridae, Paramyxoviridae, Picomaviridae, Reoviridae (Reouirus and Rotavirus), Retroviridae, Rhabdoviridae, and Togaviridae: DNA VIRUS GROUP: Adenoviridae, Herpesviridae and Iridoviridae. In addition to the viral diseases which have been internationally recognised, this review gives new information on other diseases including Salmonid Picomalike Viruses, Landlocked Salmon Virus (LSV), Atlantic Salmon Rotavirus (ASR), Trout Strawberty Disease (TSD) , Coho Salmon Tumor Virus (CSTV), Epizootic Epitheliotropic Disease of Lake Trout, Epizootic Hematopoietic Necrosis (EHN) of Trout, Erythrocytic Inclusion Body Syndrome (EIBS) . Intraerythrocytic Viruslike Particles different from EIBS in Atlantic Salmon, and Third Erythrocytic Virus associated with anemia. Among these, the pathologic conditions from which a causative virus has been isolated are Coho Salmon Tumor, Epizootic Hematopoietic Necrosis of Trout, Trout Strawberry Disease, Atlantic Salmon Rotavirus Disease, and Landlocked Salmon Virus Disease. Furthermore, Salmonid Picomalike Virus and Cutthroat Trout Virus have been isolated from the asymptomatic condition. The rest are viral infections with the viruses visualized but not yet isolated. This article deals with over twenty viruses, viral diseases and pathologic conditions of salmonids. Kqvwords: Viruses; Viral diseases; Salmonids - general

* Present address: Department Taipei, Taiwan 10764, ROC.

of Zoology,

National Taiwan University,

Fisheries Science Building,

Rm. 206,

0044-8486/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved XYDIOO44-8486(94)00372-6

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1. Introduction Wolf divided the contents of his book into four parts, in which he reviewed and discussed: Part I, Isolated Viruses and Resulting Diseases; Part II, Viral Infection of Indeterminate Pathogenicity; Part III, Viruses Visualized but Not Yet Isolated; Part IV, Viruslike Particles. The salmonid viruses and viral diseases are divided as follows: in Part I Herpesuirus salmonis Disease, Infectious Hematopoietic Necrosis, Oncorhynchus masou Virus, and Viral Hemorrhagic Septicemia; in Part II Chinook Salmon Paramyxovirus and Chum Salmon Reovirus; in Part III Atlantic Salmon Swim Bladder Sarcoma Virus, Pacific Salmon Anemia Virus and Viral Erythrocytic Necrosis; in Part IV Atlantic Salmon Papillomatosis and Rainbow Trout Intraerythrocytic Virus. This article reviews and discusses viral pathogens and viral diseases of salmonid fish only, and uses Wolfs system of grouping the agents. However, in addition to the abovementioned viruses, further information of new agents and the diseases they cause is also included in this review. Consequently, in this article, viral pathogens and viral diseases of salmonid fish are comprehensively compiled as follows.

2. Division of viral pathogens, viral diseases and pathologic conditions of salmonids

Part Z Isolated Viruses and Resulting

Viral Diseases

Section Z Diseases and Agents of Moderate to High Virulence

Coho Salmon Tumor Virus (CSTV; Igari et al., 1991) Epizootic Hematopoietic Necrosis (EHN) of Rainbow Trout (Langton Herpesvirus salmonis Disease Infectious Hematopoietic Necrosis (IHN) Infectious Pancreatic Necrosis (IPN) Nerka Virus Towada Lake, Akita & Aomori (NeVTA) Oncorhynchus masou Virus (OMV) Viral Hemorrhagic Septicemia (VHS) Yamame Tumor Virus (YTV) Section ZZDiseases and Agents of Low Virulence Trout Strawberry Disease (TSD; Fleury et al., 1985) Part ZZViral Infections of Indeterminate Pathogenicity Atlantic Salmon Rotavirus (ASR: Dopazo et al., 1990) Chinook Salmon Paramyxovirus Chum Salmon Reovirus (CSV) Landlocked Salmon Virus (LSV; Hsu et al., 1989) Salmon Picornalike Virus (McDowell et al., 1989) Steelhead Herpesvirus (SHV) Part ZZZ Viruses Visualized but Not Yet Isolated Atlantic Salmon Swim Bladder Sarcoma Virus Epizootic Epitheliotropic Disease of Lake Trout (Bradley et al., 1989) Erythrocytic Inclusion Body Syndrome (EIBS) Pacific Salmon Anemia Virus

et al., 1988)

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Third Erythrocytic Virus Associated with Anemia (Hedrick et al., 1987) Viral Erythrocytic Necrosis (VEN) Part IV Pathologic Conditions and Viruslike Particles Atlantic Salmon Papillomatosis Intraerythrocytic Viruslike Particles in Atlantic Salmon (Thorud et al., 1990) Rainbow Trout Intraerythrocytic Virus

3. Commentary

and discussion

This section deals with twelve subjects of virus, viral disease or pathologic condition of salmonids all of which have been recently described; Salmon Picornalike Virus, Landlocked Salmon Virus (LSV). Atlantic Salmon Rotavirus (ASR), Trout Strawbetry Disease (TSD), Coho Salmon Tumor Virus (CSTV), Epizootic Epitheliotropic Disease of Lake Trout, Epizootic Hematopoietic Necrosis (EHN) of Rainbow Trout, Cutthroat Trout Virus (CTV), and four pathologic conditions associated with intraerythrocytic virus or viruslike particles; Pacific Salmon Anemia Virus, Erythrocytic Inclusion Body Syndrome (EIBS), Intraerythrocytic Virus Particles in Atlantic Salmon, and Third Erythrocytic Virus Associated with Anemia. 3.1. Salmon Picornalike Virus

The virus has been isolated from ovarian fluids of cutthroat trout, rainbow trout, brown trout and brook trout. The CPE (cytopathic effect) by the virus is characterized by an area of diffuse necrosis in CHSE-214 cells. The virus does not cause any detectable disease (Yun and Hedrick, 1989). 3.2. Landlocked Salmon Virus (LSV)

A new reolike virus was isolated from landlocked salmon, Oncorhynchus masou Brevoort, and designated as landlocked salmon virus by Hsu et al. ( 1989). The typical plaguelike syncytial CPE occurred in AS, BF-2, BB, CC0 and CHSE-214 cells. The RNA electrophoretic pattern of LSV is closer to that of CSV, but the virion protein pattern is closer to that of 13P2. 3.3. Atlantic Salmon Rotavirus (ASR) ASR has been isolated from Atlantic salmon, Salmo salar, in Canada and the USA, respectively (unpublished). CPE was slow to develop in EPC and BB cell lines, but occurred rapidly in CTSE-214 cells at both 15C and 20C (Dopazo et al., 1990). 3.4. Trout Strawberry Disease (TSD)

Strawberry Disease (SD) is a subacute non-debilitating and non-fatal inflammatory skin disease of rainbow trout which was recognized in Washington State in the 1950s. Since

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then, SD has been observed in Oregon, Nevada, Idaho, Montana and California. Morbidity in some fish farms ranged up to 80%, thus causing considerable economic losses (Olson et al., 1985). An adenolike virus was isolated from the skin lesions of SD in chorioallantoic membranes of embryonated eggs. The inoculated membranes showed pock marks 1 mm in diameter. The virus showed an icosahedral symmetry; total number of capsomeres was 252; no spike was observed; the structure had a diameter about 65 nm without envelope. This is the first reported isolation of adenolike virus from a fish (Fleury et al., 1985). 3.5. Coho Salmon Tumor Virus (CSTV) CSTV is a herpesvirus isolated from the tissue of the basal cell carcinoma developed on the mouth parts of coho salmon, Oncorhynchus kisutch (Sano, 1988). It is lethally pathogenic and oncogenic to chum salmon, 0. keta, kokanee, 0. nerka, and coho salmon, 0. kisutch. Igari et al. ( 1991) showed that the NeVTA, YTV, and CSTV could be genetically identical even though they had been isolated from different host fish, and concluded that these three viruses should be treated as an intraspecific isolate. W.D. Eaton et al. (1991) found that HPV, Herpesvirus salmonis, and steelhead herpesvirus (SHV) are most likely different strains of the same virus, as are OMV and YTV although the latter two viruses are less related to one another than HPV is to SHV. Furthermore, NeVTA is related to, but clearly distinct from, OMV and YTV according to the results of the DNA hybridization assays of five salmonid herpesviruses. Their study also suggests that the salmonid herpesvirus can thus be classified as follows; Salmonid herpesvirus type 1 (HPV and SHV from North America) and Salmonid herpesvirus type 2 (OMV YTV and NeVTA from Japan). Thus, the present author applies this classification and nomenclature from now on. 3.6. Epizootic Epitheliotropic Disease of Lake Trout

This epizootic was first reported by Bradley et al. ( 1988). During the past 4 years cumulative mortalities of unknown etiology of hatchery-reared juvenile lake trout, Saluelinus namaycush, in the Great Lake Region, have exceeded 15 million individuals. Environmental conditions, ectoparasites and known microbial agents were not the cause of the mortalities. Lesions associated with the epizootics induced hyperplasia and hypertrophy of branchial and skin epithelium, renal tubule degeneration and dilation of glomeruli. A virus isolated from moribund lake trout measured 110 nm in diameter. The virus did not multiply in EPC, FHM, RTG-2, CHSE-214 and RTH-149 cell lines. Horizontal transmission was demonstrated by cohabiting healthy juvenile lake trout with the moribund fish at a water temperature of 10C. The trial fish exhibited clinical signs of whirling, ataxia and hyperexcitability, and died lo-15 days post-cohabitation. Rainbow trout, brook trout, and brown trout, Salmo trutta, were refractory. The virus was tentatively classified as a herpesvirus and named Epizootic Epitheliotropic Disease Virus. 3.7. Epizootic Hematopoietic Necrosis (EHN) of Rainbow Trout

Epizootic Hematopoietic Necrosis (EHN) of Rainbow Trout is an iridovirus infection of cultured rainbow trout in Australia reported by Langdon et al. (1988). Transmissible

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CPE typical of EHNV were produced in all RTG-2 cell cultures in 30-48 h. A vacuolating encephalopathy of variable extent and severity was usually present in affected animals. Renal hematopoietic necrosis and necrosis of gastrointestinal epithelium were prominent. Mortality was only about 0.05% per day in the 0 + fish but cumulative mortality approached 100%. Atlantic salmon are also susceptible to EHNV (Langdon et al., 1988). B.T. Eaton et al. (1991) confirmed the designation from the number and complexity of proteins in purified EHNV and the order of appearance of virus-specific protein in infected cells, and also from four other viral proteins. 3.8. Cutthroat Trout Virus (CTV) This virus was isolated from ovarian fluids of adult rainbow trout, cutthroat trout (0. clarki), brown trout (Salmo trutta), and brook trout (Saluelinus fontinalis) and from the kidney and spleen of juvenile brook and brown trout in CHSE-214 cells at 15C by Hedrick et al. ( 1991). Virions purified were hexagonal with a mean diameter of 37.5 nm and did not possess an envelope. Nucleic acid type was RNA. There was no virus-induced mortality but virus was recovered for periods of up to 3-5 weeks post-waterborne exposure of rainbow trout, brown trout and kokanee salmon (0. nerka). The following are four pathologic conditions associated with intraerythrocytic viruslike particles. A brief comparison among them is given in Table 1.
Table 1 Comparison Pathologic

virus or

among four novel erythrocytic and epizootic condition

viruses of salmonids Cytoplasmic + inclusion Transmission _ Virus 80 nm Toga

Infected organelle Membraneenclosed in cytoplasm Associated with membrane of internal organelles IVAl /space between nucleus and cytoplasm. IVA2f cytoplasmic cavity between them Membrane-bound vacuoles in cytoplasmic or perinuclear space

Pacific Salmon Anemia: Severe anemia/Coho, chinook/Oregon, USA EIBS: Serious anemia/chinook/ Pacific N.W., USA

+ 0.8-3 pm

+ chinook, coho, rainbow

15 nm ssRNA Toga

Intraerythrocytic Viruslike Particles: Atlantic Salmon/ Norway

no data

IVAl 80 nm IVA2 90 nm

Third Erythrocytic Virus Assoc. Anemia: Severe anemia, degeneration of hematopoietic tissue, etc./ coho/Califomia, USA

+ l-2 pm

no data

106 nm

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3.9. Pacijc Salmon Anemia Virus Since Holt and Rohovec ( 1984) reported anemia of coho salmon, 0. kisutch, in Oregon, and Leek (1985) demonstrated artificial transmission of erythrocytic virus, no new information has been available. This virus is an 80-nm particle found in the cytoplasm of erythrocytes of juvenile and yearling coho salmon and of spring chinook salmon, 0. tshawytscha, resulting in serious losses due to the severely anemic condition. The virus was experimentally transmittable to healthy fall chinook salmon by force feeding via stomach incubation. From the size, chloroform sensitivity, and cytoplasmic replication, this virus could be a member of the Togavirus group. The affected fish had a high incidence of external fungus at or near the dorsal or caudal fin or on the snout and were distributed along the sides of the raceway (Holt and Rohovec, 1984). 3.10. Erythrocytic Inclusion Body Syndrome (EIBS)

Erythrocytic inclusions in the blood of spring chinook salmon are the first confirmed occurrence of a natural infection caused by an erythrocytic necrosis virus in a population being reared in freshwater (Leek, 1987). The erythrocytic inclusion bodies ranged in size from 0.8 to 3 pm. The viral particles averaged 75 nm in diameter and they were scattered randomly in the cytoplasm (Leek, 1987). Pelton ( 1987) dealt with horizontal transmission trials of EIBS by placing EIBS-negative coho salmon into live boxes below two raceways of known EIBS-positive chinook salmon. His experimental results suggested that EIBS could be transmitted horizontally from chinook salmon to coho salmon. Infected fish were detected after 85-l 12 days at water temperatures ranging from 5 to 7C. Piacentini et al. (1989) also demonstrated that under laboratory conditions, the virus of EIBS was transmitted horizontally, and rainbow trout and cutthroat trout, 0. clarki, could be infected by injection. The disease in these species was, however, less severe than in coho salmon and chinook salmon. Piacentini and Rohovec ( 1989) concluded that the genome of EIBS virus is ssRNA, because the inclusion bodies, which electron microscopy had shown to contain mature enveloped virions in the cytoplasm, fluoresced red in the blood smear stained with acridine orange. Arakawa et al. ( 1989) also were able to transmit the virus to healthy coho salmon by injection of microbe-free 220 nm filtrates and were able to find similar virus particles in the blood of artificially infected fish. They considered that the EIBS virus is most likely a member of the Togaviridae, from the size and shape of the virion, the presence of an electron-dense centre, the possession of a lipid envelope, and the association with membranes of internal organelles. Takahashi ( 1992) studied comprehensively EIBS in cultured coho salmon in Japan and elucidated the following points: epizootics of EIBS in coho salmon in seawater, the methods of artificially inducing EIBS; progression of EIBS in artificially induced coho salmon; relation between the growth of coho salmon and the progression of EIBS; the susceptibility of coho salmon according to size, and of several other species of salmonids; the natural occurrence of EIBS in juvenile coho salmon reared in freshwater; and the resistance to reinfection and immune response. However, since comprehensive histopathological study of EIBS is lacking, comparative pathology cannot be reviewed between EIBS and the following pathologic conditions.

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Thorud and Djupvik ( 1988) also reported infectious anemia in Atlantic salmon, Salmo salar, which is characterized by severe anemia, a chronic course and high mortality, and exophthalmia, congestion, hypertrophied liver with necrosis and spleen with hemosiderin in acutely affected fish; ascites and extreme pallor of the gills and internal organs in peracutely affected cases. Histopathological examination reveals focal or zonal hepatic necrosis. Hematological examination shows the extreme reduction of the number of circulating leucocytes and erythrocytes. This epizootic has spread in Norway since 1984. The pathologic condition was transmitted to healthy parr by intraperitoneal injection with liver homogenate from typically affected fish and to control fish by cohabitation with injected fish. However, there is no description of virus and inclusion bodies in the smears, in this paper, and also no discussion of whether this pathologic condition was connected with EIBS. The first detection of viruslike particles similar to EIBS from Atlantic salmon in Norway was reported by Lunder et al. ( 1990). The particles were five- or six-sided with diameter of about 75-100 nm and were found in erythrocytes of both freshwater and saltwater salmon suffering from anemia and moderate to high mortalities. As far as the virus diameter, morphology, and erythrocytic inclusion bodies are concerned, there are no significant differences between chinook salmon (Leek, 1987) and Atlantic salmon cases. 3.11. Intraerythrocytic Viruslike Particles in Atlantic Salmon

Two intraerythrocytic viruslike particles different from EIBSV in Atlantic salmon in Norway were reported by Thorud et al. ( 1990). These particles were referred to intraerythrocytic viruslike particles in Atlantic salmon, IVAl and IVA2. Both IVAl and IVA2 were observed in erythrocytes from the salmon from fish farms during outbreaks of infectious anemia (Thorud and Djupvik, 1988). IVAl measured about 80 nm in diameter, particles were spherical to hexagonal in shape and appeared within the space between the nucleus and cytoplasm. IVA2 was about 90 nm in diameter and was observed in what appeared to be cavities in the cytoplasm. Both IVAl and IVA2 showed no cytoplasmic inclusion bodies. Although there are significant differences in pathologic condition, host species, and inclusion body formation between rainbow trout intraerythrocytic virus reported by Landolt et al. (1977) and IVAl or 2, the respective viruslike particles cannot be distinguished by size. The organelles in which the respective particles were observed are similar; the former in intraerythrocytic vesicles, the latter in what appeared to be acytoplasmic cavity or vesicle. 3.12. Third Erythrocytic Virus Associated with Anemia

A third erythrocytic virus associated with anemia was reported by Hedrick et al. ( 1987). This virus was found in coho salmon reared in saltwater in California and suffering from severe anemia (PCVs down to 10%). No other microbial agents were detected, only the virus. Histopathological examination showed a diffuse degeneration of the hematopoietic tissues and heavy deposits of hemosiderin in the melanomacrophage centre in the kidney and spleen. Blood smears from affected fish showed the formation of rod-shaped erythrocytic cytoplasmic inclusion bodies ranging in size from 1 to 2 pm. The examination of erythrocytes by electron microscopy showed numerous viruslike particles with a consistent

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tissues and heavy deposits of hemosiderin in the melanomacrophage centre in the kidney and spleen. Blood smears from affected fish showed the formation of rod-shaped erythrocytic cytoplasmic inclusion bodies ranging in size from 1 to 2 pm. The examination of erythrocytes by electron microscopy showed numerous viruslike particles with a consistent size of 106 nm in diameter within membrane-bound vacuoles in the cytoplasmic or perinuclear space.

4. Conclusion of the bisegmented ds RNA virus group (Birnaviridae) and Aquarwas recognized by the International Committee on Taxonomy of Viruses (Classification and Nomenclature of Viruses edited by Francki et al., 1991) . Furthermore, a new classification of salmonid herpesvirus was proposed by W.D. Eaton et al. ( 199 1) ; Salmonid herpesvirus type 1 and type 2. Consequently, the foregoing viruses, viral diseases and pathologic conditions of salmonids are at present classified in families and groups as shown in Table 2. Furthermore, unclassified viruses and pathologic conditions of salmonids are as follows: The establishment
eovirus (a genus in the Reoviridae)
Atlantic Salmon Papillomatosis Table 2 Family Bimaviridae Paramyxoviridae Picomaviridae Reoviridae Aquareovirus Rotavirus Retroviridae Rhabdoviridae Lyssavirus Togaviridae RNA virus group Infectious Pancreatic Necrosis Virus (IPNV) Chinook Salmon Paramyxovirus Salmonid Picomalike Virus Chum Salmon Reovirus (CSV) Landlocked Salmon Virus (LSV) Atlantic Salmon Rotavims (ASR) Atlantic Salmon Swim Bladder Sarcoma Virus Infectious Hematopoietic Necrosis Virus (IHVN) Virus Hemorrhagic Septicemia Virus (VHSV) Pacific Salmon Anemia Virus Erythrocpic Inclusion Body Syndrome (EIBS) Virus DNA virus group Trout Strawberry Disease (TSD) Virus Epizootic Epitheliotropic Disease Virus of Lake Trout Salmonid Herpesvims Type 1 (Herpesvirus salmonis HPV: Steelhead Herpesvirus, SHV) Salmonid Herpesvirus Type 2 (Nerka Virus Towada Lake, Akita & Aomori, NeVTA; Oncorhynchus masou Virus, OMV; Yamame Tumor Virus, YTV; Coho Salmon Tumor Virus, SCTV) Epizootic Hematopoietic Necrosis Virus (EHNV) of Rainbow Trout Viral Erythrocytic Necrosis Virus (VENV)

Family Adenovitidae Herpesviridae

Iridoviridae

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Thorud, K.E., Lunder, T., Wiik, S. and Engeland, E., 1990. Electron microscopic observations of EIBSV-like particles different from EIBSV in Atlantic salmon, Salmo salar, in Norway. Bull. Eur. Assoc. Fish Pathol., 10: 95-97. Wolf, K., 1988. Fish Viruses and Fish Viral Diseases. Cornell University Press, New York, x +476 pp. Yun, S. and Hedrick, R.P., 1989. A picomalike virus from salmonid fishes in California. Am. Fish. Sot. Fish Health Sect. Newsl., 17: 6.