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1 CAB INTERNATIONAL 1999. Fish Diseases and Disorders, Volume 3:Viral, Bacterial and Fungal Infections(eds P.T.K. Woo and D.W. Bruno)

1Infectious Pancreatic Necrosis and

Associated Aquatic Birnaviruses

P.W. Reno

Coastal Oregon Marine Experiment Station, Department of Microbiology,

Laboratory for Fish Disease Research, Mark O. Hatfield Marine Science

Center, Newport, Oregon 97365-5296, USA.

INTRODUCTION

Infectious pancreatic necrosis (IPN) is a disease which causes high mortalities inyoung salmonid fishes; the aetiological agent of the disease (IPNV) was the firstvirus to be isolated from teleosts (Wolf et al.,1960). In the three decades sincethat work, agents biochemically and serologically identical to IPNV theaquatic birnaviruses have been detected in a wide variety of both diseased andnon-diseased fishes and other aquatic animals.

The early work on IPNV was mainly responsible for the development of fishvirology. Techniques for the isolation of viruses from teleosts were modifiedfrom methods used for the isolation of mammalian viruses. However, we nowknow that IPNV and its interactions with the host are unique in several respects.

1. The virus itself has sufficiently unusual biophysical characteristics to warrantits place as the archetype of a new family of viruses, the birnaviruses (Dobos etal., 1979).2. The carrier state associated with IPNV infection is unique among animaldiseases. The infection is lethal only to young animals, although virus can bereadily isolated in high concentrations from the viscera of infected fish during

the lifespan of the host, and there is no significant disease recrudescence, as inherpetic infections, etc.3. Serologically and biochemically related viruses induce a variety of diseasesyndromes in taxonomically diverse host groups, which also include aquaticinvertebrates. The worldwide distribution of these viruses in cultured as well aswild fishes and shellfish provides significant potential for economic damage.

Infectious pancreatic necrosis and other birnavirus-induced diseases cancause a significant economic impact on cultured fishes, especially salmonids.The cost can be as a consequence of lethal disease in young-of-the-year fish, orthe destruction of infected stocks even in the absence of disease. The virus isvertically transmitted; therefore, the detection of virus in broodstock, even in the

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2 P.W. Reno

absence of disease, often means the destruction of these valuable animals. Evenas recently as the late 1980s, there were instances in the USA where 7 millionyoung salmonids were destroyed to eliminate IPNV from a single hatchery (P.Walker, Colorado, 1988, personal communication) and others where detection of

the virus in returning coho salmon resulted in the destruction of 2 million eggs(Olson et al., 1994); similar occurrences were also reported in Canada (B.Larson, Alberta, 1988, personal communication). In addition, regulationscurrently in place to reduce the dissemination of diseases of salmonids oftenresult in restriction of the movement of IPNV carrier fish between local, regionaland/or national boundaries. These restrictions have attendant adverse economicconsequences to aquaculturists. In many instances, the slaughter of infected fishand/or the restriction of movement of fish may be more economicallydetrimental than the loss associated with direct mortalities.

The mandated destruction of salmonid stocks and restriction of movementdue to IPNV are controversial. From one perspective, the disease itself is nothighly destructive, although it has been in the past, and therefore need not beregulated. Since only swim-up fry and fingerlings are generally affected, theimpact of the disease can be ameliorated by spawning additional brood fish tocompensate for the potential loss caused by the disease. Another perspective isthe dissemination into watersheds of a virus unresponsive to therapeutic agentswhich can readily infect susceptible native or cultured stocks in adjacentdrainages. Given the myriad variables which come into play in the generation ofIPN and the potential for extensive, irreparable damage to stocks, it would seemprudent to adhere to more stringent rather than lax requirements. Resolution ofthe problem of IPNV management will be difficult and achieved only through a

thorough knowledge of the epizootiology of the disease and an adequatedatabase on both the disease and the virus. Many of these are unknown atpresent.

Infectious pancreatic necrosis virus may also have an economic impact onaquaculture because of fish health inspections on certain stocks of fish. Due tothe occult nature of the infection, these inspections are frequently mandatedprior to the movement or sale of fish across local, regional and nationalboundaries. Tests required for the detection of IPNV and other teleost virusesoften represent a large out-of-pocket expense for aquaculturists. Again, this canbe a contentious issue because the regulations are not often applied uniformly,

even within regions regulated by one agency.With the advent of molecular biological techniques, researchers are close tothe development of a vaccine for IPN, but the intricate lifestyle of the virus mayprovide a considerable stumbling-block to disease prophylaxis. Future methodsdesigned to control the disease worldwide will also be difficult, given the ubiqui-tous nature of the agent. Only the most stringent controls on the movement ofcultured fish, based on detection of the virus by the most sensitive and specificdiagnostic techniques, will lead to the successful elimination of this pathogen.

A number of reviews have been published on IPN disease and IPNV. Theextensive publication base includes more than 150 printed articles in the lastdecade. In this review, I shall include more recent data and integrate information

into a logical summary.

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3Infectious Pancreatic Necrosis

THE DISEASES AND AGENTS

Aquatic birnaviruses are the most pervasive pathogens of aquatic animals. Theyhave been isolated from teleosts as well as aquatic invertebrates of freshwater,

brackishand sea-water environments. The ubiquitous nature of these agents andthe lack of association with disease have led to difficulty in nomenclature. Inorder to maintain a consistency in this review, the term IPNV virus will be usedstrictly to describe those isolates which have been shown to produce disease insalmonids and aquatic birnaviruses will be used for those which are eitherassociated with other disease states or have not been shown to be the causalagents of naturally or experimentally induced disease in aquatic animals.

HOST RANGE

Disease

Early reports of IPNV were limited to epizootics in cultured brook trout,Salvelinus fontinalis(Wood et al., 1955; Snieszko et al., 1957, 1959; Wolf et al.1960). With the development of several continuous cell lines from teleost fishes(Wolf and Quimby, 1962; Wolf and Mann, 1980) and as more laboratoriesbecame more proficient in the use of cell lines, it was found that IPNV wasresponsible for disease in a variety of salmonid species, including members ofthe genera Salmo, Salvelinus and Oncorhynchus. During the early 1970s, IPNcaused high mortalities in European and Japanese rainbow and brown trout (Ball

et al., 1971; Sano, 1971; Vestergrd-Jrgensen and Kehlet, 1971). Morerecently, epizootics of diseases not characteristic of salmonid IPN have beenassociated with birnavirus infections in epizootic proportions (Table 1.1).

The first report of birnavirus-induced disease in non-salmonids was inJapanese eels (Anguilla japonica), first sampled in 1969 (Sano et al., 1981). Thisdisease of cultured eels was characterized as branchionephritis. Experimentalinfection with the virus (eel virus European (EVE)) indicated that the branchiallesions were probably due to supervening bacterial infections and that thedisease should be referred to as eel nephritis. Neutralization studies indicatedthat the aetiological agent was a birnavirus which is serologically related to the

Sp (from Spjarup, Denmark) serotype of IPNV. Another birnavirus-induceddisease which caused mortalities in Japanese fish caused ascites in yellowtail,Seriola quinqueradiata (Sorimachi and Hara, 1985). The condition was in feralfry used as seed stock for mariculture. Because clinical signs occurred in fry, thedisease is similar to IPN. In addition, mortalities occurred in another flat-fishspecies from Japan, the Japanese flounder (Paralichthys olivaceus). Fish held inculture facilities died from ascites and cranial haemorrhage. An aquaticbirnavirus was isolated from moribund fish and an ascitic disease wasexperimentally induced by intraperitoneal injection of the virus from moribundfish showing either disease syndrome (Kusuda et al., 1989).

Stephens et al. (1983) isolated an aquatic birnavirus from the brain and other

tissues of menhaden (Brevoortia tyrranus) with spinning disease, a perennial

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4 P.W. Reno

Ta

ble

1.

1.

Naturaldiseasesc

ausedby,orassociatedwith,aquaticbirnaviruses.Include

dareisolationsofaquaticbirnavirusesin

theabsenceofsubstantiveproofofcausalassociationwithdisease.

Di

sease

Species

Mortalities

Behavio

uralsigns

Grosssigns

Microscopiclesions

Reference

Di

seasesforwhichRiverspostulateshavebeenfulfilled

Infectious

Salmonids

095%

Whirling,anorexia

Blackening,

Focalcoagulative

1

p

ancreatic

abdominaldiste

nsion,necrosisofexocrine

n

ecrosis

petechiainviscera,

andendocrine

yellowexudate

ingut

pancreas,kidney,

intestine

Tu

rbot

Scophthalmus

Notreported

Whirling,anorexia,Musclehaemorrhage,Coagulativenecrosis

2

h

aemopoietic

maximus

letharg

y,surface

anaemicgillsan

d

ofhaemopoietic

n

ecrosis

swimm

ing

liver,nofoodin

gut

elementsofkidney,

focalnecrosisofliver

Ye

llowtail

Seriola

High

Nonere

ported

Ascites,catarrh,

Coagulativenecrosis

3

a

scites

quinqueradiata

haemorrhageofliver,

ofpancreaticacinar

d

isease

stomachandpy

loric

cells,kidneytubular

caeca;palesple

en,

epithelia,and

kidney,gills

hepatocytes

Ee

lnephritis

Anguilla

5075%

Bodysp

asms

Retractedabdom

en,

Proliferative,

4

anguillaand

andrig

idity

reddeningofan

alfin,

exudative

Anguilla

abdomen,gills;

glomerulonephritis,

japonica

ascites,kidney

tubulardegeneration

;

enlargement

focalnecrosisofliver

andspleen

Sp

inning

Brevoortia

Natural,

Spinning

Haemorrhageat

fin

Degenerationofbasal

5

d

iseaseof

tyrranus

unknown

base,gills,eyes

;

layerofepidermis

m

enhaden

Experimental,

darkening

withpyknosis

100%

Ja

panese

Paralichthys

560%

None

Ascites,cranial

Nonereported

6

flounder

olivaceus

haemorrhage

a

scites

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Di

seasesforwhichbirnaviruseshavebeenisolatedfrommo

ribundanimals

Se

abass

Dicentrarc

hus

90%

Spiralswimming

Exophthalmia,

Delaminationof

7

ne

phritis

labrax

distensionofswim-

intestinalepithelium

bladderandgall-

bladder

Stripedbass

Morone

High

Darting

swimming;None

Degenerationof

8

mortality

saxatilis

headup

atrest

epidermalbasal

layer;pan-necrosis

Milkfishulcer

Chanosch

anos0

None

Ulcerativenecrosis

Nonedescribed

9

disease

ofskin

Da

bascites

Limanda

0

None

Ascites

Nonedescribed

10

limanda

Unnamed

Paralichthys

Unknown

Notreported

Notreported

Notreported

11

ep

izootic

lethostigm

a

Ee

l

Anguilla

0

None

Stomatopapillom

a

Papilloma

12

stomatopapilloma

anguilla

Ku

murashrimp

Penaeus

2643%

Lethargy,difficulty

Erosivenecrosis

of

Nonereported

13

disease

japonicus

inmoulting

thoraciclimbsan

d

uropods

Clamgill

Meretrix

0

None

Darkenedgills

Necrosisofgilltissue

14

ne

crosis

lusoria

Unnamed

Tellinaten

uis

0

None

Chalky,brittlesh

ell

Nonereported

15

1,

Woodetal.,1995;2,Castricetal.,1987;3,Sorimachiand

Hara,1985;4,Sanoetal.,1981;5,Stephensetal.,1981;6,

Ku

sudaetal.,1989;7,Bonamietal.,1988;8,Schutzetal.,1984;9,Chenetal.,1990;10,D

iamantetal.,1988;11,McAllisteret

al.,1984;12,NagabayashiandWolf,1979;13,Giorgetti,1990;14,Loetal.,1991;15,Hille

tal.,1982.

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6 P.W. Reno

high-mortality disease in the Chesapeake Bay region of the eastern USA. Thevirus was isolated in a cell line from the same species (Stephens, 1981). Thedisease was experimentally induced in susceptible menhaden afterintraperitoneal injection of the virus. Subsequent attempts to isolate the same

virus from diseased menhaden in other teleost continuous cell lines wereunsuccessful. Since the original menhaden cell line was lost, there have been nofurther isolations of the virus from diseased or non-diseased fish.

In each of these cases, Rivers postulates have been fulfilled, indicating thatthe aetiological agents of the diseases were aquatic birnaviruses whichcross-reacted serologically with IPNV. In several other instances, birnaviruseshave been isolated from aquatic animals undergoing epizootic disease, but as yetthere has not been irrefutable evidence that the isolated birnaviruses were causalagents (Table 1.1).

A birnavirus infection was associated with haematopoietic necrosis andcaused high mortalities in turbot (Scophthalmus maximus) held at 18C in seawater on the coast of France (Castric et al., 1987). Within 15 days after transferfrom fresh water to sea water, cumulative mortalities reach 25%, but nomortalities occurred in the same population of fish held at the freshwater site. Nodefinitive studies have been done to confirm Rivers postulates for this diseaseand a birnavirus is suspected.

In addition to a birnavirus isolated from Japanese eels with nephritis (Sanoet al., 1981), a birnavirus was also isolated in Japan from eels exhibitingstomatopapillomas (Nagabayashi and Wolf, 1979). Although the virus wasisolated from moribund fish, there was no indication that the virus was capableof producing the papillomatous lesions in homologous animals.

Transmitting papillomas in homoeotherms in often difficult, and the strongassociation of the papilloma group of viruses with this disease in other animalsmakes it unlikely that a birnavirus was the causal agent in eels. In retrospect, it ispossible that the eels affected with the stomatopapillomas were adventitiouscarriers of the virus (Sano et al., 1981)and the isolated aquatic birnavirus had noinvolvement in the development of papillomas.

An aquatic birnavirus belonging to the Sp (European) serotype was isolatedfrom visceral organs of snakehead fish (Ophicephalus striatus) and eyespot barb(Hampala dispar) undergoing episodes of ulcerative disease in Thailand andLaos (Wattanavijarn et al., 1988). Again, there is no further information to

indicate that this agent was responsible for the syndrome.Another birnavirus was isolated from sea bass (Dicentrarchus labrax) offthe coast of France (Bonami et al., 1983) during a severe epizootic, in whichmortalities reached 95%. There was no evidence of bacterial infection orparasites in the moribund fish, but again it is uncertain whether the virus ismerely associated with the mortality or was the aetiological agent.

With the rather large exception of IPN disease, the disease syndromes thathave been strongly associated with aquatic birnaviruses (yellowtail ascites,Japanese flounder disease syndromes, eel nephritis, spinning disease ofmenhaden and turbot renal necrosis) occur in marine animals or in those thatspend the bulk of their life in sea water. The IPN which affects the anadromous

Salmo and Oncorhynchus also fits into this category, although the susceptible

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stage occurs in fresh water rather than in the marine environment. Recently,postsmolt salmon died from an IPN-like disease in marine cage culture;however, there was a confounding infection with the agent of pancreas diseaseof an IPNV (Smail et al., 1992). Although the titres of virus from moribund fish

were not reported, titres were approximately 104

g1

tissue 4 weeks after theepizootic. This is low compared with the titres in trout succumbing to IPNdisease (Wolf et al., 1969; Reno, 1976).

It is likely that diseases caused by aquatic birnaviruses are more extensive innature because reports of this family of viruses are primarily in cultured animals,which have economic importance. Relatively little information is availableregarding birnavirus infections in wild populations of aquatic animals that arenot of commercial importanceand this is unlikely to change unless some of theseanimals develop commercial importance.

Virus

Birnaviruses are the most ubiquitous pathogenic microorganisms in aquaticspecies. During the 1960s, following on the heels of Wolfs early work on theisolation and characterization of IPNV, many investigators detected the virus insalmonids, especially those undergoing epizootics of frank disease. During the1970s and 1980s, with closer scrutiny of cultured and wild non-salmonids, manyisolations of aquatic birnaviruses were made from a large number of aquaticanimals.

In the first report on birnaviruses in non-salmonids, Sonstegrd et al. (1972)

detected IPNV in common suckers (Catostomus commersoni) with no clinicaldisease. They were resident in a tailway of a trout hatchery with perennial IPNepizootics. It is a highly probable that the viruses in the suckers were from thefish in the hatchery. Since that time, birnaviruses have been detected in nearly 80species of aquatic animals (Table 1.2). Although these viruses belong to the sameserotype as IPN, most isolations were from apparently healthy animals.Infectivity experiments have rarely been conducted to determine if the isolateswere capable of replicating in the homologous host. Most often only biophysicaland serological characterizations of the isolate were performed to confirm thatthe agent was a birnavirus. There was little information on the virulence of these

viruses.Several authors have attempted to determine if the isolates from non-salmonid species are capable of inducing IPN disease in trout. It is difficult toevaluate these experiments since a variety of exposure protocols were used.Several investigators have standardized techniques for inducing IPN disease inaquatic birnaviruses (Bootland et al., 1986; McAllister and Owens, 1986). Insome cases, aquatic birnaviruses from non-salmonids could produce classicIPN disease in salmonids (Table 1.3). In 1965, Yasutake et al. demonstrated thatIPNV isolated from rainbow trout caused overt disease in chinook salmon(Oncorhynchus tshawytscha). However, the birnaviruses from eels wereincapable of inducing disease in trout, although they were virulent in the

homologous species, A. japonica (Sano et al., 1981). Similar results were

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8 P.W. Reno

Ta

ble

1.

2.

Speciesofaquatic

animalsfromwhichbirnaviruseshavebeenisolated.

Class

Family

Genusandspecies

Commonname

Reference

Monogonta

(Order)Ploima

Branchio

nusplicatilis

Rotifer

27

Mollusca

Veneridae

Meretrix

lusoria

Enamelvenusshell

1

Veneridae

Corbicularfluminou

Asianclam

30

Acmae

idae

Patellavulgata

Scallop

2

Littorin

idae

Littorina

littorea

Periwinkle

2

Mytilid

ae

Mytiluse

dulis

Mussel

2

Ostreid

ae

Crassostreavirginica

Americanoyster

2

Ostreid

ae

C.gigas

Japaneseoyster

2

Ostreid

ae

Ostreaedulis

Europeanoyster

2

Tellinid

ae

Tellinate

nuis

Tellina

3

Veneridae

Mercenariamercenaria

Surfclam

2

Crustacea

Portunidae

Carcinus

maenas

Shorecrab

2

Portunidae

Macropipusdepurator

Harbourcrab

2

Penaeidae

Penaeus

japonicus

Japaneseshrimp

4

Ag

natha

Petrom

yzontidae

Lampetrafluviatilis

Lamprey

5

Teleostei

Clupeidae

Brevoortiatyrranus

Menhaden

6

Clupeidae

Dorosom

acepedianum

Gizzardshad

25

Anguillidae

Anguilla

japonica

Japaneseeel

7

Anguillidae

A.rostrata

Americaneel

25

Anguillidae

A.anguilla

Europeaneel

8

Esocidae

Esoxlucius

Northernpike

9

Esocidae

E.niger

Chainpickerel

10

Salmonidae

Huchohucho

Grayling

10

Salmonidae

Oncorhynchusmykiss

Rainbowtrout

11

Salmonidae

O.

keta

Chumsalmon

12

Salmonidae

O.

kisutch

Cohosalmon

13

Salmonidae

O.clarki

Cutthroattrout

12

Salmonidae

O.

tshaw

ytchka

Chinooksalmon

12

Salmonidae

O.gorbu

scha

Pinksalmon

12

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Salmonidae

O.rhodu

rus

Amagotrout

14

Salmonidae

Salvelinu

sfontinalis

Brooktrout

15

Salmonidae

S.naymacush

Laketrout

16

Salmonidae

S.alpinu

s

Arcticchar

12

Salmonidae

Salmosa

lar

Atlanticsalmon

16

Salmonidae

S.

trutta

Browntrout

17

Salmonidae

Thymallu

sthymallus

Grayling

18

Salmonidae

Prosopiu

mwilliamsoni

Whitefish

28

Channidae

Ophicephalusstriatus

Snakeheadfish

18

Cyprinidae

Abramis

brama

Bream

2

Cyprinidae

Barbodesschwanefeldi

Barb

10

Cyprinidae

Bliccabjoerkna

Dace

17

Cyprinidae

Carassiusauratus

Goldfish

20

Cyprinidae

C.ceratis

inis

Carp

10

Cyprinidae

C.carass

ius

Carp

2

Cyprinidae

Chondrostomanasus

Nase

10

Cyprinidae

Cyprinus

carpio

Commoncarp

2

Cyprinidae

Gobiogo

bio

Goby

10

Cyprinidae

Oxyeleotrismarmoratus

Sandgoby

29

Cyprinidae

Hampala

dispar

Eyespotbarb

18

Cyprinidae

Phoxinusphoxinus

Dace

5

Cyprinidae

Rutilusrutilus

Roach

2

Cyprinidae

Scardiniuserythrophthalmus

Rudd

10

Cyprinidae

Barbusb

arbus

Barbel

10

Cyprinidae

Brachydaniorerio

Zebradanio

10

Cobitid

ae

Misgurnusanguillicaudatus

Roach

20

Atherin

idae

Menidiamenidia

Silversides

22

Sciaenidae

Leiostom

usxanthurus

Drum

22

Carang

idae

Seriolaq

uinqeradiata

Yellowtail

21

Cichlidae

Symphysodondiscus

Discus

22

Cichlidae

Tilapiam

ossambica

Tilapia

10

Percida

e

Percaflu

viatilis

Yellowperch

5

Continuedover

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10 P.W. Reno

Percich

thyidae

Dicentrarchuslabrax

Seabass

29

Percich

thyidae

Moronesaxatilis

Stripedbass

24

Poeciliidae

Xiphophorusxiphidium

Platy

10

Gadida

e

Gadusm

orhua

Atlanticcod

2

Pleuronectidae

Limanda

limanda

Commondab

26

Pleuronectidae

Paralichthyslethostigma

Southernflounder

25

Pleuronectidae

Pleurone

ctesfluviatis

Sole

2

Pleuronectidae

Hippoglo

ssushippoglossus

Halibut

29

Pleuronectidae

Scophthalmusmaximus

Turbot

25

1,Loetal.,1991;2,Hilletal.,1982;3,Hill,1976;4,Bovoetal.,1984;5,Munroetal.,1976;6,Stephensetal.,1983;7,S

anoetal.,

1981;8,Hudsonetal.,1981;9,Ahne,1979;10,Ahneetal.,1989b;11,Parisotetal.,1963;12,Wolf,1988;13,WolfandP

ettijohn,

1970;14,Sano,1973;15,Hedric

ketal.,1986a;16,MacKelvie

andArtsob,1969;17,Wolfetal.,1960;18,Wattanavijarnetal.,1988;

19,Ahne,1980;20,Hill,1982;21,Chenetal.,1984;22,Sorim

achiandHara,1985;23,Ada

irandFerguson,1981;24,Wechsleret

al.,1986b;25,McAllisteretal.,1984;26,Castricetal.,1987;27,Compsetal.,1991;28,YamamotoandKilistoff,1979;2

9,Bonami

et

al.,1983;30,T.Hstein,personalcommunication.

Ta

ble

1.

2.

Continued.

Class

Family

Genusandspecies

Commonname

Reference

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reported in isolates from striped bass (Wechsler et al., 1986b), flounder(McAllister and McAllister, 1988) and oysters (Hill et al., 1982).

GEOGRAPHICAL RANGE

Disease

While the disease was evidently first described from the Maritime Provinces,Canada (MGonigle, 1940),and soon thereafter in the eastern USA (Wood et al.,1955), it was later noted in many areas of the western USA (Yasutake et al.,1965), especially in rainbow trout and brook trout transferred from the easternUSA. Epizootics in rainbow trout with signs of IPN disease reported in France(Besse and de Kinkelin, 1965) were caused by an aetiological agent which wasserologically distinct from the North American serotype (Wolf and Quimby,1971). The detection of IPN in France was followed by diagnosis ofdisease in rainbow trout in Denmark (Vestergrd-Jrgensen and Bregnballe,1969), Norway (Hstein and Krogsrud, 1976), Sweden (Ljungberg andVestergrd-Jrgensen, 1973), the UK (Ball et al., 1971), Germany (Schlotfeldtet al., 1975) and Italy (Ghittino, 1972). Outside Europe, the disease has beendocumented in the Far East, usually in fish imported from enzootic areas or infish cohabiting the same water source as infected imported fish. The virus hasbeen isolated from Japan (Sans, 1971), Korea (Hah et al., 1984), Taiwan(Hedrick et al., 1983a China (Jiang et al., 1989) and Thailand and Laos(Wattanavijarn et al., 1988).

Virus

The isolation of aquatic birnaviruses from various geographical areas hasincreased markedly since the isolation of IPNV from the eastern USA (Wolf etal., 1960). In a few instances, there has been sufficient epizootiological evidenceto support the orderly spread of the virus from region to region. The ubiquitousnature of aquatic birnaviruses on a worldwide scale is indicated in Figs 1.1, 1.2and 1.3. When the viruses were serotyped, they proved to be serologically

identical to serotypes of IPN from epizootics (Caswell-Reno et al.,1986; Hilland Way, 1995).These agents have been isolated from regions where salmonids are reared

and from areas without salmonids. The data are often difficult to access andsummarize easily because of the inconsistent nature of the published literatureand the variety of sources from which samples have been taken. The presence ofthese viruses in feral animals is a confounding factor. Since little currentinformation about the distribution of aquatic birnaviruses is available in theliterature, an attempt has been made in this review to update the information(Figs 1.11.3).

Prior to the late 1980s, the virus was present in most areas of North America.

In many areas, the prevalence levels were low, but in some areas (Maritime

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12 P.W. Reno

Ta

ble

1.

3.

Virulenceofaquaticbirnavirusesinexperimentalinfectionsofhomologousa

ndheterologoushosts.

Serot

ypeofvirus,

ifr

eported,

inparentheses.

Species

Sizeof

Routeof

Doseperf

ish

Specific

Durationo

f

Iso

latefrom

infected

host

exposure

(TCID50)

mortality(%)observatio

nReference

Ho

mologousspeciesinfected

Salvelinusfontinalis

S.

fontinalis

Fry

IMM

Notreported

7

98

14d

1

S.fontinalis

S.

fontinalis(NB)

0.5g

IMM/15min

106.9/ml

3

1y

2

S.fontinalis

S.

fontinalis(Penn-2

)

5mo

IP

106.3

0

25d

3

S.fontinalis

S.

fontinalis(VR-2

99)

6mo

IP

106.3

0

25d

3

S.fontinalis

S.

fontinalis(VR-2

99)

14mo

IP

106.3

0

25d

3

On

corhynchusmykiss

O.mykiss

0.1

1g

IMM./

1h

104.8

15

90d

4

O.

mykiss

O.myki

ss(Sp)

5

7cm

IMM.

105.0

20

21d

5

O.

mykiss

O.mykiss(Ab)

5

7cm

IMM.

105.0

0

21d

5

O.

mykiss

O.mykiss(Ab)

0.2g

IMM.

104

9

35d

6

O.

mykiss

O.myki

ss(Sp)

0.2g

IMM.

104

42

35d

6

Salmosalar

S.salar

Fry

IMM.

105

108

0

15

30d

7

Brevoortiatyrranus

B.

tyrranus

5

25cm

IP

105

100

7d

8

An

guillajaponica

A.

japonica

10g

IP

107.8

5.5

75

NR

4

Paralichthysolivaceus

P.olivac

eus

5g

IP

Notreported

60

21d

9

Misgurnus

M.angu

illicaudatus

10

15g

IP

104

75

7d

11

anguillicaudatus

Mo

ronesaxatilis

Morone

saxatilis

5d

6mo

Oral,IMM.

102

106

0

33w

12

Seriolaquinqueradiata

S.quinqueradiata

On

corhynchusmykiss

Salvelin

usfontinalis

25mm

IMM.

Notreported

42

51

20d

12

(Sp)

O.

mykiss

Salmos

alar(Sp)

Fryparr

IMM.

105

108

0

1.5

30d

7

O.

mykiss

O.

tshawytscha

2

3in

SC

103

100

200 kDa) which had the electrophoreticmobility, and an immunoelectrophoretic pattern and reactivity with rabbitantitrout antisera characteristic of trout immunoglobulin (Reno, 1976; Dorson etal., 1989). The neutralizing antibody was evident at 30 days postinfectionand

remained for several years (de Kinkelin et al., 1984). Hill and Way (1983) foundthat IPNV vaccine inactivated by -propriolactone was not as effective asformalized virus in protecting trout. It has been suggested that there is aninverse correlation between IPNV titres in tissues and serum antibody titres(Wolf and Quimby, 1969; Yamamoto, 1975a), but there is no statisticalcorrelation (Reno, 1976; analysis of data from Hedrick and Fryer, 1982).Unfortunately, nothing is known of the levels of neutralizing antibody whichare necessary to prevent disease and/or infection, or whether animals with highserum antibody titres are susceptible to superinfection with the same ordifferent serotypes.

The situation becomes more complicated as a non-induced, non-immunoglobulin anti-IPNV molecule with a 6S sedimentation coefficient wasfound in the serum of normal trout (Scherrer et al., 1974; Hill and Dixon, 1977;Kelly and Nielson, 1985). The 6S-sensitive virus strains generated in vitroareless virulent than 6S-resistant strains (Kelly and Nielson, 1985). The natureand significance of this substance is unknown, but it may have a naturalprotective effect. Gonzalez et al. (1989) determined that anti-trinitrophenolantibodies in rainbow trout inhibit the replication of IPNV in vitro. In addition,immunosuppression of IPNV-infected carrier trout with corticosteroids did notpromote viral replication or the induction of frank disease, although humoralimmunity was eliminated (Bucke et al., 1979; Bootland et al., 1986, Etchberger,

1987).

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Another component of resistance to IPN is interferon, a broad-rangingprotective molecule generated by lymphocytes and other cells. In vitrointerferon production has been demonstratedand there is a correlation betweenthe optimal temperature for cell growth, maximal interferon production and

virus titre (Scherrer et al., 1974). Interferon has been demonstrated in serum oftrout infected with the virus (de Kinkelin et al., 1982), although its in vivosignificance is not known.In vitro, it has been shown that the cell density has aneffect on the virus yield, with cultures plated at higher densities producing moreinterferon and concomitantly less virus (Okamoto et al., 1983b).

Little research has been done to examine the role of cell-mediated immunityin protection against clinical IPN disease. There is some information thatsuggests that there is a cellular response to the virus in carrier fish. Knott andMunro (1986) demonstrated that Atlantic salmon inoculated with IPNV had adepressed level of leucocytic mitogenesis to phytohaemagglutinin anddecreased number of natural cytotoxic cells (NCC). Similarly, Tate et al.(1990)determined that, in addition to the alterations of mitogenesis and NCC,experimentally-infected rainbow trout had higher titres of virus in adherent,surface immunoglobulin-positive (Sig+) cells than in non-adherant Sig cells.This indicates a greater affinity of the virus for B-cell lineages than T-celllineages. Etchberger (1987) indicated that cytokinins are elicited fromleucocytes of natural IPNV carrier fish as well as fish experimentally infectedwith IPNV. Macrophage migratory inhibition factor was also produced in thepresence of IPNV. Natural cytotoxic cells may also play a role in the non-specific response to IPNV infection, since Moody et al. (1985) found thatcontinuous teleost cell lines infected with IPNV were more sensitive to the

cytolytic action of trout leucocytes than were uninfected cells.

TOPICS FOR FURTHER STUDY

There has been a distinct emphasis on the characterization of the virus. Futurestudies should include the following.

1. Vaccine development. Prophylaxis holds the best hope for elimination ofbirnavirus diseases from aquaculture. Despite considerable research efforts in

the past 30 years, no efficacious vaccine against IPN or any other fish viraldisease has been produced commercially, although some successes have beennoted in the laboratory. However, with the advent of new techniques inbiotechnology, it may be possible to develop a subunit vaccine which isenviromentally innocuous and effective in protecting fish from aquaticbirnaviruses.2. A better understanding of the nature of the carrier state. The mechanism(s)responsible for the generation and maintenence of the IPN carrier state isunknown. Vaccines which simply reduce or eliminate mortalities will do little tosolve the problem of IPN on a worldwide scale. They must not only alleviatedisease, but also prevent infection and the development of carriers.

3. Mortalities due to IPNV in adult salmon. The emergence in European

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Atlantic salmon culture of high mortality in postsmolt salmon may indicate adifferent virulence mechanism(s) or new strains of virus that are responsible forthe mortalities. It is important to try to discern differences between the strains ofvirus causing postsmolt mortalities and those of the same serotype which only

instigate mortalities in juvenile fish.4. Improved diagnostic methods.Although the methods currently used for thedetection and identification of the aquatic birnaviruses are sensitive and specific,they are based on cell culture isolation followed by identification, both of whichinvariably consume much time and technical effort. Simpler, more rapidtechniques would improve the lot of fish health specialists desperately seekingviruses.5. Update information on aquatic birnavirus diseases other than IPN.Severaldiseases caused by aquatic birnaviruses can have a significant impact onaquaculture of non-salmonid species. Virtually nothing is known about thesediseases except that they are associated with aquatic birnaviruses. In thosecountries where these diseases occur, it behoves investigators to expand theirinformation base about these diseases. In addition, this would aid inunderstandiing the processes by which aquatic birnaviruses infect fish and causedisease.6. Assess the effects of management techniques in controlling the disease. Giventhe expansive geographical and host range of aquatic birnaviruses, managementthrough direct action at facilities or restrictions on fish movement can have amarked impact on promulgation of the disease. In Europe, especially, where IPNis enzootic, this type of approach would be helpful. This can be done locally withattention to the use of uncontaminated water sources and disinfectant methods

and especially the use of virus-free stocks. Even in areas where IPN is rampant,perhaps some initial small scale efforts are required to establish stocks ofvirus-free fish in hatcheries fish.

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