viral erythrocytic necrosis
Don't need the entire report?
Generate a print friendly version containing only the sections you need.Generate report
PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- viral erythrocytic necrosis
International Common Names
- English: piscine erythrocytic necrosis; viral erythrocytic necrosis of salmonids
OverviewTop of page
Viral erythrocytic necrosis (VEN), first described by Laird and Bullock (1969) as piscine erythrocytic necrosis (PEN), is a disease of marine fish characterized by erythrocytic degeneration and the presence of cytoplasmic inclusion bodies (viroplasms) in circulating erythrocytes (Evelyn and Traxler, 1978; Reno et al., 1978). Reports of similar conditions in amphibians and reptiles, combined with reports of VEN in fishes from around the world, suggest that the reported cases are likely caused by a group of related aetiological agents. For a long time, the inclusions were suspected to be caused by blood parasites, but evidence of a viral aetiology was first reported in reptiles (Stehbens and Johnston, 1966). The viral nature of the disease in fish was later demonstrated by electron microscopy studies indicating association of icosahedral virus particles within affected erythrocytes (Appy et al., 1976; Walker and Sherburne, 1977). The associated virus has been referred to as erythrocyte necrosis virus (ENV) (Haney et al., 1992), but fulfillment of Koch’s Postutales is currently precluded by the refractory nature of the virus to established cell lines.
The disease has now been reported in more than 20 species of marine and anadromous fish, in both wild and cultured populations (Smail, 1982). The disease is not usually associated with high mortality, but it has been reported to occur epizootically in Pacific herring (Meyers et al., 1986). Transmission experiments have verified the infectious nature of the disease. Blood smears from affected fish reveal a single inclusion body in the cytoplasm of erythrocytes, visible by light microscopy. A virus belonging to the icosahedral cytoplasmic deoxyribovirus (ICDV) group and presumptively classified as an iridovirus has been associated with the inclusion bodies (Appy et al., 1976; Reno et al., 1978).
Viral erythrocytic necrosis is not considered to be a severe or economically important fish disease. The current research on VEN is low compared with that on other viral diseases in fish and most of the information was published in the late 1970s and 1980s.
[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.]
Hosts/Species AffectedTop of page
A wide variety of marine fish species from the northern parts of the Atlantic and Pacific Oceans are affected. These include Atlantic cod (Laird and Bullock, 1969; Appy et al., 1976; Reno and Nicholson, 1981), blenny (Johnston and Davies, 1973), Atlantic (Reno et al., 1978) and Pacific (Meyers et al., 1986) herring and the Pacific salmonids, chum, pink, coho, chinook salmon and steelhead trout (Evelyn and Traxler, 1978; Rohovec and Amandi, 1981; Bell and Traxler, 1985). Viral erythrocytic necrosis has also been observed in the southern Pacific Ocean, namely in coho salmon in Chile (Reyes and Campalans, 1987). It has been reported in cultured eel in Taiwan (Chen et al., 1985), and is suspected to affect several marine species in coastal waters off Portugal, including Madeira (Eiras, 1984; Eiras et al., 1996). Thus, VEN has a wide geographical distribution and is not confined to special fish groups occupying particular ecological niches.
Experimental induction of VEN in Atlantic cod (Reno et al., 1986) and in several Pacific salmonids - Atlantic salmon, rainbow trout, brown trout and brook trout (MacMillan and Mulcahy, 1979) - has been described. The transmission experiments have confirmed field observations that the susceptibility to VEN in salmonids is age- and species-dependent. For example, juveniles <1 g are more susceptible than larger fish. No signs of VEN are observed in large coho salmon and rainbow trout 6 months after infection. Furthermore, in experiments with juveniles, erythrocytic inclusion bodies characteristic of VEN appear earlier in chum salmon, brown trout and brook trout (2 days p.i.) than in pink, coho, sockeye and chinook salmon and rainbow trout (5-7 days) (MacMillan and Mulcahy, 1979).
Basic virological and pathological research with VEN is limited because of the refractory nature of the presumed aetiological agent to established cell lines; consequently, risk factors predisposing susceptible populations to the disease are largely presumed from case history reports. Exposure of Pacific herring to suboptimal environmental conditions, including reduced salinity, increased fish density, and predator harassment was believed to exacerbate latent infections with ENV, resulting in several related epizootics in Pacific herring from Alaska (Meyers et al., 1986).
Laboratory studies indicate that infected salmonids experience physiological and haematological changes that may increase susceptibility to secondary pathogens and decrease physiological tolerances to environmental stressors. Mortality rate following challenge with Vibrio anguillarum is 2.6× greater and mean time to death is shorter in chum salmon with VEN than in uninfected cohorts. Additionally, VEN may act as an exacerbating stressor contributing to mortality of Pacific herring that are co-infected with viral haemorrhagic septicaemia virus and Ichthyophonus hoferi (Hershberger et al., in press). Oxygen concentration present when ENV-infected chum salmon die is significantly greater (3.9 mg l-1) than in uninfected cohorts (1.6 mg l-1). Similarly, osmoregulatory metrics including serum sodium and potassium are more variable in VEN infected chum salmon and may result in osmoregulatiry difficulty, especially when smolts outmigrate to seawater (MacMillan et al., 1980).
DistributionTop of page
VEN is typically considered to be a condition of marine fishes. The wide geographical distribution of VEN includes the northern and southern Pacific Ocean, and northern Atlantic Ocean (Dannevig and Thorud, 1999). Reported hosts include Atlantic cod (Laird and Bullock, 1969; Appy et al., 1976; Reno and Nicholson, 1981), blenny (Johnston and Davies, 1973), Atlantic (Reno et al., 1978) and Pacific (Meyers et al., 1986) herring and the Pacific salmonids, chum, pink, coho, chinook salmon and steelhead trout (Evelyn and Traxler, 1978; Rohovec and Amandi, 1981; Bell and Traxler, 1985). Viral erythrocytic necrosis has also been observed in the southern Pacific Ocean, namely in coho salmon in Chile (Reyes and Campalans, 1987). It has been reported in cultured eel in Taiwan (Chen et al., 1985), and is suspected to affect several marine species in coastal waters off Portugal, including Madeira (Eiras, 1984; Eiras et al., 1996). Thus, VEN has a wide geographical distribution and is not confined to special fish groups occupying particular ecological niches.
Distribution TableTop of page
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Atlantic, Northeast||Present||Dannevig and Thorud, 1999|
|Atlantic, Northwest||Present||Laird and Bullock, 1969; Appy et al., 1976; Walker and Sherburne, 1977; Sherburne and Bean, 1979; Reno and Nicholson, 1981; Dannevig and Thorud, 1999|
|Mediterranean and Black Sea||Present||Pinto et al., 1989|
|Pacific, Northeast||Present||Evelyn and Traxler, 1978; MacMillan and Mulcahy, 1979; Groberg et al., 1982; Meyers et al., 1986; Dannevig and Thorud, 1999|
|Pacific, Northwest||Present||Dannevig and Thorud, 1999|
|Pacific, Southeast||Present||Reyes and Campalans, 1987|
|Japan||Present||Present based on regional distribution.|
|-Hokkaido||Present||Yoshimizu et al., 1988|
|Taiwan||Present||Chen et al., 1985|
|Canada||Present||Present based on regional distribution.|
|-British Columbia||Present||Evelyn and Traxler, 1978|
|-New Brunswick||Present||Sherburne, 1973; Appy et al., 1976; Walker and Sherburne, 1977; Sherburne and Bean, 1979|
|-Newfoundland and Labrador||Present||Reno and Nicholson, 1981|
|-Nova Scotia||Present||Sherburne and Bean, 1979|
|Greenland||Present||Reno and Nicholson, 1981|
|USA||Present||Present based on regional distribution.|
|-Alaska||Present||Meyers et al., 1986|
|-Maine||Present||Sherburne, 1973; Sherburne, 1977; Walker and Sherburne, 1977; Reno et al., 1978; Sherburne and Bean, 1979; Reno and Nicholson, 1980|
|-Massachusetts||Present||Walker and Sherburne, 1977; Sherburne and Bean, 1979|
|-New Hampshire||Present||Sherburne and Bean, 1979|
|-Oregon||Present||Rohovec and Amandi, 1981; Groberg et al., 1982|
|-Washington||Present||MacMillan and Mulcahy, 1979|
|Chile||Present||Reyes and Campalans, 1987|
|Portugal||Present||Eiras, 1984; Eiras et al., 1996|
|-Madeira||Present||Eiras, 1984; Eiras et al., 1996|
|Spain||Present||Pinto et al., 1989|
|UK||Present||Johnston and Davies, 1973; Smail and Egglestone, 1980|
PathologyTop of page
Pathological consequences of VEN are most readily observed in erythroid cells, most obviously observed as cytoplasmic inclusions. Infected cells demonstrate single, round, acidophilic cytoplasmic inclusion bodies, ultimately lyse, and are replaced in circulation by erythrocytic ghost cells. Erythroblasts can become multinucleated and begin to predominate the profile of circulating cells. Additionally, erythroblasts in the pronephros may contain up to seven nuclei. Hypersegmented neutrophils, containing as many as nine nuclear lobes, may appear in circulation. Myelocytic cells become rare. Other abnormalities in erythroblasts include megablastoid nuclear appearance with particulate chromatin; multinucleation and signs of nuclear degeneration including, pyknotic, karyorrhetic, and karyorrhexic nuclei; and irregular cell margins (Reno and Nicholson, 1981, Reno et al., 1986 and MacMillan et al., 1989).
The pink or magenta cytoplasmic inclusions, typically 0.5-5 µm diameter (Laird and Bullock, 1969), seen in Giemsa-stained blood smears of Pacific salmon are assumed to be virion aggregates (see below) and viral precursor material (viroplasm) (Appy et al., 1976; Evelyn and Traxler, 1978). In Atlantic cod, the inclusions are frequently surrounded by punctiform bodies less than 0.5 µm in diameter. Non-membrane-bound electron-dense viroplasms are often associated with virions (Nicholson and Reno, 1981). Two types of inclusions are seen in electron micrographs of infected erythrocytes from Pacific herring (Reno et al., 1978). One (measuring 1.5 µm) is non-membrane-bound and appears to be associated with virus, while the other type (diameter from 0.5 to 3 µm) is membrane-bound but not virus-associated.
Cellularity of the kidney cells changes little, even in heavy VEN infections. Viral inclusions can be detected in the pronephros of the kidney, and all stages of morphologically identifiable erythroblasts ultimately demonstrate inclusions. Groups of erythroblasts surrounding a central macrophage are sometimes present in impressions from haematopoietic tissues. Hypersegmented neutrophils can be detected in haematopoietic tissue.
The infection results in moderate anaemia in cod and herring (Reno et al., 1985), while a more severe anaemia (haematocrit values < 5) develops in experimentally infected Pacific salmonids (MacMillan and Mulcahy, 1979) and Pacific herring (Hershberger et al., in review). Haemolytic anaemia, with haemosiderosis and erythroblastosis, has been decribed in moribund Pacific herring (Meyers et al., 1986). Erythroblastosis can also be observed in experimentally infected Atlantic cod (Reno et al., 1986) and chum salmon (MacMillan and Mulcahy, 1979).
Viral erythrocytic necrosis mortality is usually low, but may increase in association with vibriosis or bacterial kidney disease (Evelyn and Traxler, 1978). High mortality associated with epizootics of VEN has only been reported in Pacific herring (Meyers et al., 1986). Experimentally infected chum salmon had increased mortality, due to vibriosis, decreased tolerance to depletion of oxygen and reduced osmoregulatory ability in sea water (MacMillan et al., 1980). However, no increased mortality was observed in experimentally infected Atlantic cod, although a reduced resistance to stress was reported (Nicholson and Reno, 1981).
DiagnosisTop of page
Presumptive diagnosis for VEN is by examination of Leishman-Giemsa (Wedemeyer and Yasutake, 1977) stained blood films for presence of cytoplasmic inclusions. The refractory nature of the presumed aetiological agent to established cell lines precludes isolation by standard virological isolation followed by identification by standard immunological or serological procedures. Additionally, difficulties in amplifying ENV DNA using primers from conserved regions of the iridovirus genome currently limit the utility of the polymerase chain reaction as a confirmation tool (Hershberger and Emmenegger, unpublished data). Depending on the stage of infection, the virus particles may not necessarily be in close proximity to the cytoplasmic inclusion. Confirmation of VEN is based on observation of icosahedral-shaped virus particles with electron microscopy. It should be cautioned that erythrocytic inclusions in fish erythrocytes are not pathognomonic for VEN. Differentiation from erythrocytic inclusion body syndrome (EIBS), a condition associated with erythrocytic inclusion bodies primarily in freshwater fishes, can be made by staining blood films with acridine orange; VEN inclusions stain green and EIBS inclusions stain orange (Thoesen, 1994).
Clinical signs of VEN include general maladies associated with poor fish health and are not considered pathognomonic. The most consistent clinical sign includes anaemia, evident as pale gills and internal organs, resulting from erythrocyte degeneration. Other signs in some affected hosts may include unilateral or bilateral exophthalmia and dark green colored livers. In Pacific herring, external haemorrhages have been associated with VEN infections (Rohovec and Amandi, 1981), but may have been a lingering sign of previous infection with viral haemorrhagic septicaemia virus (Hershberger et al., in review). Until Koch’s postulates have been performed, these clinical signs should not necessarily be attributed to VEN.
List of Symptoms/SignsTop of page
|Finfish / Change in colour - Eyes||Aquatic:Adult||Sign|
|Finfish / Change in colour - Eyes||Aquatic:Adult||Sign|
|Finfish / Darkened coloration - Skin and Fins||Aquatic:Fry||Sign|
|Finfish / Gall bladder, dark green liquid - Organs||Aquatic:Adult||Sign|
|Finfish / Generalised lethargy - Behavioural Signs||Aquatic:Adult||Sign|
|Finfish / Haemorrhagic lesions - Skin and Fins||Aquatic:Fry||Sign|
|Finfish / Liver dark green - Organs||Aquatic:Adult||Sign|
|Finfish / Mortalities -Miscellaneous||Aquatic:Adult,Aquatic:Fry||Sign|
|Finfish / Paleness - Gills||Aquatic:Adult||Sign|
|Finfish / Periorbital oedema - Eyes||Aquatic:Adult||Sign|
|Finfish / Pop-eye - Eyes||Aquatic:Adult||Sign|
|Finfish / Rolling Motion - Behavioural Signs||Aquatic:Fry||Sign|
Disease CourseTop of page
VEN is considered a chronic disease, often taking weeks or months to develop heavy infections. Although a single description of VEN-induced mortality in wild fish is documented (Meyers et al., 1986), mortality occurring as a direct result of VEN is generally considered negligible (Evelyn and Traxler, 1978). However, elevated mortality can occur with concomitant infections of Rennibacterium salmoninarum, Vibrio sp. (Evelyn and Traxler, 1978 and MacMillan et al., 1980), viral haemorrhagic septicaemia virus, or Ichthyophonus hoferi (Hershberger et al., in review), or exposure to suboptimal environmental conditions (MacMillan et al., 1980 and Haney et al., 1992).
Progression of VEN in susceptible hosts is characterized by the presence of cytoplasmic inclusions in affected erythrocytes; however, kinetics and intensity of the disease progression is dependent upon host species and size. Time required for cytoplasmic inclusions to appear after IP injection of ENV-infected blood inoculum ranges from 2 days in chum brook and brown trout fry, 4-5 days in pink, coho and sockeye salmon, and 7days in rainbow trout. Among all species, time to first appearance of cytoplasmic inclusions increases with fish age until inclusions never develop in the largest coho salmon and rainbow trout (MacMillan and Mulcahy, 1979). The disease progresses rapidly in juvenile chum salmon (0.5 g), where single, acidophilic cytoplasmic inclusions, often adjacent to the nucleus, are present in 40-60% of the erythrocytes after 2 days. The percentage of infected mature erythrocytes increases with time, reaching 80% after 2 weeks and 90% after 1 month (MacMillan et al., 1979). Severity of ENV infection, characterized by extensive leucocytosis including decreased erythrocyte counts, haematocrits, and haemoglobin concentrations, peaks 3-4 weeks post infection (Haney et al., 1992). As the disease progresses in chum salmon and Pacific herring, the proportion of circulating erythroblasts increases until all circulating red blood cells are represented by blast cells, and inclusion bodies are present in 80% of the erythroblasts 1 month p.i. Cytoplasmic inclusions are seen in all stages of morphologically identifiable erythroblasts in the pronephros 2-4 weeks p.i., indicating that ENV infects erythroblasts in the kidney prior to their release into circulation (MacMillan et al., 1989). The occurrence of circulating multinucleate, giant erythroblasts, abnormal erythroid cell maturation and phagocytosis of abnormal erythroblasts by macrophages indicates both virally mediated erythroid cell destruction and ineffective erythropoiesis. Gross signs of infection appear 1 month post-infection and are characterized by signs of anaemia including gill pallor and pale internal organs. Clotting time for whole and recalcified blood is significantly longer in VEN-infected fish from 1 to >7 months post exposure (MacMillan et al., 1989).. The rapid disease progression occurring in chum salmon is similar to that described in Pacific herring (MacMillan and Mulcahy, 1979, Hershberger et al., in review)
In larger chum salmon (75-150 g), an experimentally induced VEN infection also results in haematological changes, such as reduced number of erythrocytes, increased proportion of immature erythrocytes and extensive leuocytosis (Haney et al., 1992). The course of haematological changes indicates that the peak of infection occurs between 3 and 4 weeks p.i., while recovery starts after 5 weeks. In the same study, it is concluded that a VEN infection does not cause development of a stress response. The mean cortisol level in infected fish was only slightly elevated during a 5-week period, and no increase in plasma glucose and lactate or reduction in liver glycogen could be observed. Plasma proteins and osmolality were unchanged (Haney et al., 1992).
In contrast to its progression in chum salmon, VEN develops much more slowly in Atlantic cod. Cod challenged with sonicated blood from diseased fish develop cytoplasmic inclusions 40 days post infection. The proportion of infected erythroblasts increases and may reach 100% 3 months after infection. Subsequently, the infection in immature erythrocytes decreases while prevalence of inclusions in mature erythrocytes increases to approximately 40-60%. A significant erythroblastosis occurs, but, in the cod, there is no evidence for infection of newly generated erythrocytes (Reno et al., 1986). Among confined wild cohorts, <0.01% of erythrocytes initially demonstrate inclusions, and prevalence of inclusions increases slowly with confinement time, peaking at 40% after 3 months confinement. Prevalence of necrotic erythrocytes decreases to 20% after 4 months and they disappear after several months. Erythroblastosis occurs during the course of infection, peaking at the same time as the VEN infection rate. Immature erythrocytes are the first cells to demonstrate infection, and evidence of necrosis occurs more rapidly than in mature erythrocytes. Nearly 100% of erythroblasts are infected during the peak of infection (approximately 1 month post confinement); the prevalence of inclusioned erythroblasts then decreases quickly (Reno et al., 1986).
No changes of plasma electrolytes occur in VEN-infected cod, suggesting that the infection has no impact on the osmoregulatory capacity (Reno et al., 1985). Erythrocytes from infected fish lyse more rapidly than those from uninfected fish when kept in isotonic media (Nicholson and Reno, 1981), but an increase in fragility in hypotonic media has not been demonstrated (Reno and Nicholson, 1980; Haney et al., 1992).
EpidemiologyTop of page
VEN literature is predominated by surveys and case histories documenting prevalences in populations; consequently, epidemiological information describing disease transmission and kinetics is limited. Waterborne transmission of the disease to naïve hosts has been demonstrated, with erythrocytic inclusions appearing in chum salmon 1 month after exposure and in brook trout 7 days after exposure (MacMillan and Mulcahy, 1979). Additional evidence of waterborne-transmission exists in juvenile Pacific herring, where prevalence and intensity of VEN increases from undetectable levels when the fish were captured to 100 % infection prevalence with >90 % of erythrocytes demonstrating inclusions after 12 days of confinement in laboratory tanks (Hershberger et al., in review). Presumptive evidence exists for vertical transmission of ENV, indicated by the presence of VEN-like inclusions in hatchery-reared chum and coho salmon alevins originating from VEN-positive adults (Rohovec and Amandi, 1981; Schiewe et al., 1988). In fish injected with ENV, time to development of VEN is dependent upon the host species, with erythrocytic inclusions appearing after 1-2 days in chum salmon and brook/brown trout; 4-5 days pink, coho, sockeye, and Chinook salmon; and 7 days in rainbow trout fry (MacMillan and Mulcahy, 1979, MacMillan et al., 1989). Resulting disease, characterized by anaemia and low haematocrits persists for > 40 days in chum salmon (MacMillan and Mulcahy, 1979, Haney et al., 1992), and > 55 days in Pacific herring (Hershberger et al., in review). Within a given host species, infectivity is inversely related to host size (MacMillan and Mulcahy, 1979, Smail and Egglestone, 1980), with older cohorts possibly becoming resistant to infection.
Prevalence of VEN in affected wild populations varies from 1% to 90%, depending on species and geographical location of fish. The prevalences were 1.5% and 3% in North Atlantic cod and North Pacific herring, respectively (Reno and Nicholson, 1981; Traxler and Bell, 1988). In another study, up to 60% of Pacific herring were infected, and young fish had a higher prevalence than adult fish within a region (MacMillan and Mulcahy, 1979). During a 5-month holding period, the prevalence of VEN in Pacific herring increased from 3% to 70% (Traxler and Bell, 1988). More than 80% of a chum and pink salmon population may be infected (Evelyn and Traxler, 1978).
Impact SummaryTop of page
|Fisheries / aquaculture||Negative|
Impact: EconomicTop of page
Although VEN has been reported from aquacultured fishes, reported occurrences are generally not coincident with epidemics; therefore, the economic impact to the aquaculture industry is considered negligible.
Impact: EnvironmentalTop of page
A single report of VEN associated with mortality of wild fish currently exists in the literature (Meyers et al., 1986). An estimated 100,000 dead Pacific herring juvenile (age 1+ cohorts) were reported in a small cove in southeast Alaska during the summer of 1985, and VEN was ascribed as the presumed cause of death. Two additional VEN-associated kills occurred in southeast Alaska during the same summer, but estimates of affected fish were not reported. Although attempted viral and bacterial isolations from affected fish were unsuccessful in identifying other potentially pathogenic agents, care should be taken when ascribing causation for kills of wild Pacific herring. For example, wild Pacific herring can undergo a highly virulent epidemic of viral haemorrhagic septicaemia (VHS), and a VEN episode can follow several days later (Hershberger et al., in press). In this case, investigation of the fish kill several days after the event may result in failed isolation of VHS virus, the agent responsible for the kill, and mis-diagnosis of VEN as the cause of mortality.
Zoonoses and Food SafetyTop of page
Although difficulties with isolation and maintenance of pure cultures preclude definitive studies on the temperature tolerance, host specificity, and survivability of ENV, there is no indication that humans represent a suitable host. However, the broad range of hosts reported with VEN-like inclusions, including fishes, amphibians and reptiles, and the ease of transmission in waterborne challenge studies, dictate that diseased fish should be considered highly contagious to other non-human hosts.
ReferencesTop of page
Appy RG; Burt MDB; Morris TJ, 1976. Viral nature of piscine erythrocytic necrosis (PEN) in the blood of Atlantic cod (Gadus morhua). Journal of the Fisheries Research Board of Canada, 33(6):1380-1385.
Bell GR; Traxier GS, 1985. First record of viral erythrocytic necrosis and Ceratomyxa shasta noble, 1950 (Myxozoa: Myxosporea) in feral pink salmon (Oncorhynchus gorbuscha walbaum). Journal of Wildlife Diseases, 21(2):169-171.
Chen SN; Kou GH; Hedrick RP; Fryer JL, 1985. The occurrence of viral infections of fish in Taiwan. [European eel virus and pancreatic necrosis virus]. Fish and shellfish pathology. Proceedings of the European Association of Fish Pathologists, Plymouth, September 1983., 313-319.
Dannevig BH; Thorud KE, 1999. Other viral diseases and agents of cold-water fish: infectious salmon anaemia, pancreas disease and viral erythrocytic necrosis. Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections., 149-175.
Eiras JC, 1984. Virus infection of marine fish: prevalence of viral erythrocytic necrosis (VEN) in Mugil cephalus L., Blennius pholis L. and Platichthys flesus L. in coastal waters of Portugal. Bulletin of the European Association of Fish Pathologists, 4(3):52-56.
Eiras JC; Costa G; Biscoito M; Davies AJ, 1996. Suspected viral erythrocytic necrosis (VEN) in the intertidal fish Mauligobius maderensis from Madeira, Portugal. Journal of the Marine Biological Association of the United Kingdom, 76:545-548.
Groberg WJ; Hedrick RP; Fryer JL, 1982. Viral diseases of salmonid fish in Oregon. In: Proceedings of the North Pacific Aquaculture Symposium, August 1980, Anchorage, Alaska, 345-357.
Johnston MRL; Davies AJ, 1973. A Pirhemocyton-like parasite of the blenny, Blennius pholis L. (Teleostei; Blenniidae) and its relationship to Immanoplasma Neumann, 1909. International Journal for Parasitology, 3:235-241.
Laird M; Bullock WL, 1969. Marine fish hematozoa from New Brunswick and New England. Journal of the Fisheries Research Board of Canada, 26:1075-1102.
MacMillan JR; Mulcahy D, 1979. Artificial transmission to and susceptibility of Puget Sound fish to viral erythrocytic necrosis (VEN). Journal of the Fisheries Research Board of Canada, 36(9):1097-1101.
MacMillan JR; Mulcahy D; Landolt M, 1980. Viral erythrocytic necrosis: some physiological consequences of infection in chum salmon (Oncorhynchus keta). Canadian Journal of Fisheries and Aquatic Sciences, 37(5):799-804.
MacMillan JR; Mulcahy D; Landolt ML, 1989. Cytopathology and coagulopathy associated with viral erythrocytic necrosis in chum salmon. Journal of Aquatic Animal Health, 1(4):255-262.
Meyers TR; Hauck AK; Blankenbeckler WD; Minicucci T, 1986. First report of viral erythrocytic necrosis in Alaska, USA, associated with epizootic mortality in Pacific herring, Clupea harengus pallasi (Valenciennes). Journal of Fish Diseases, 9(6):479-491.
Pinto RM; Alvarez-Pellitero P; Bosch A; Jofre J, 1989. Occurrence of a viral erythrocytic infection in the Mediterranean sea bass, Dicentrarchus labrax (L.). Journal of Fish Diseases, 12(2):185-192.
Reno PW; Kleftis K; Sherburne SW; Nicholson BL, 1986. Experimental infection and pathogenesis of viral erythrocytic necrosis (VEN) in Atlantic cod, Gadus morhua. Canadian Journal of Fisheries and Aquatic Sciences, 43(5):945-951.
Reno PW; Nicholson BL, 1981. Ultrastructure and prevalence of viral erythrocytic necrosis (VEN) virus in Atlantic cod, Gadus morhua L., from the northern Atlantic Ocean. Journal of Fish Diseases, 4(5):361-370.
Reno PW; Philippon-Fried M; Nicholson BL, 1978. Ultrastructural studies of piscine erythrocytic necrosis (PEN) in Atlantic herring (Clupea harengus harengus). Journal of the Fisheries Research Board of Canada, 35(1):148-154.
Reyes XP; Campalans MB, 1987. Necrosis eritrocitica viral (VEN) presunta en salmon coho de la Decima region, Chile. Investigaciones Marinas, Valparaiso, 15:5-31.
Schiewe MH; Novotny AJ; Harrell LW, 1988. Viral erythrocytic necrosis of salmonids. Disease diagnosis and control in North American marine aquaculture., 339-340.
Sherburne SW, 1973. Erythrocytic degeneration in the Atlantic herring, Clupea harengus harengus L. Fishery Bulletin, 71:125-134.
Sherburne SW, 1977. Occurrence of piscine erythrocytic necrosis (PEN) in the blood of the anadromous alewife, Alosa pseudoharengus, from Maine coastal streams. Journal of the Fisheries Research Board of Canada, 34:281-286.
Sherburne SW; Bean LL, 1979. Incidence and distribution of piscine erythrocytic necrosis and the microsporidian, Glugea hertwigi, in rainbow smelt, Osmerus mordax, from Massachusetts to the Canadian Maritimes. Fishery Bulletin, 77(2):503-509.
Smail DA, 1982. Viral erythrocytic necrosis in fish: a review. Proceedings of the Royal Society of Edinburgh, B, 81(3):169-176.
Smail DA; Egglestone SI, 1980. Virus infections of marine fish erythrocytes: prevalence of piscine erythrocytic necrosis in cod Gadus morhua L. and blenny Blennius pholis L. in coastal and offshore waters of the United Kingdom. Journal of Fish Diseases, 3(1):41-46.
Stehbens WE; Johnston MRL, 1966. The viral nature of Pirhemocyton tarantolae. Journal of Ultrastructure Research, 15:543-554.
Traxler GS; Bell GR, 1988. Pathogens associated with impounded Pacific herring Clupea harengus pallasi, with emphasis on viral erythrocytic necrosis (VEN) and atypical Aeromonas salmonicida.. Diseases of Aquatic Organisms, 5(2):93-100.
Walker R; Sherburne SW, 1977. Piscine erythrocytic necrosis virus in Atlantic cod Gadus morhua, and other fish: ultrastructure and distribution. Journal of the Fisheries Research Board of Canada, 34(8):1188-1195.
Yoshimizu M; Nomura T; Awakura T; Kimura T, 1988. Incidence of fish pathogenic virus among anadromous salmonid in the notthern part of Japan (1976-1986). Sci. Rep. Hokkaido Salmon Hatchery, 42:1-20.
ContributorsTop of page
Marrowstone Marine Station, Western Fisheries Research Center, Biological Resources Discipline, (USGS), 616 Marrowstone Point Road, Nordland, WA 98358, USA
Distribution MapsTop of page
Unsupported Web Browser:
One or more of the features that are needed to show you the maps functionality are not available in the web browser that you are using.
Please consider upgrading your browser to the latest version or installing a new browser.
More information about modern web browsers can be found at http://browsehappy.com/