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    DISEASES OF AQUATIC ORGANISMS

    Dis Aquat OrgVol. Published

    INTRODUCTION

    Dating back possibly to the Middle Ages, commoncarp Cyprinus carpio in European pond culture havebee n plag ue d by a comp lex of infectious disea ses vari-

    ously known as infectious dropsy, rubella, infectiousascites, hemorrhagic septicemia, and red contagiousdisease (Hofer 1904, Schperclaus 1930, Toma$ec etal. 1964, Bauer & Faktorovich 1969). These diseasesproved to be of great economical importance, causing

    Inter-Resea rch 2002 w ww.int-res.com *Corresponding author.E-mail: [email protected]

    REVIEW

    Spring viremia of carp (SVC)

    W. Ahne1, H. V. Bjorklund2, S. Essbauer3,*, N. Fijan4, G. Kurath5, J. R. Winton5

    1Institute of Zoology, Fishery Biology and Fish Diseases, Faculty of Veterinary Medicine of the Ludwig Maximilians

    University of Munich, Kaulbachstrasse 37, 80539 Muenchen, Germany2Orion Pharma Animal Health, PO Box 425, 20101 Turku, Finland

    3WHO-centre for Comparative Virology, Institute of Medical Microbiology, Infectious and Epidemic Diseases,

    Faculty of Veterinary Medicine of the Ludwig Maximilians University of Munich, Veterinaerstr. 13, 80539 Muenchen, Germany4Department of Biology and Pathology of Fish and Bees, Veterinary Faculty, University of Zagreb, Heinzelova 55,

    PO Box 190, 10000 Zagreb, Croatia5Western Fisheries Research Center, 6505 NE 65th Street, Seattle, Washington 98115, USA

    ABSTRACT: Spring viremia of carp (SVC) is an important disease affecting cyp rinids, ma inly commoncarp Cyprinus carpio. The d isea se is widespre ad in Europe an ca rp culture, where it cause s significantmorbidity and mortality. Designate d a n otifiable disea se by the Office Inte rna tional des Epizooties, SVCis caused by a rhab dovirus, spring viremia of carp virus (SVCV). Affected fish show de struction of tissuesin the k idney, spleen and liver, lead ing to hem orrhage , loss of water-salt balance a nd impairment of im-mun e re sponse. High mortality occurs at wa ter temp eratures of 10 to 17C, typically in spring. At highe rtempe ratures, infected carp de velop h umoral antibodies that can neu tralize the spread of virus and suchcarp a re prote cted a gainst re-infection by solid immu nity. The virus is shed m ostly with the feces a ndurine of clinically infected fish a nd by carriers. Waterborne transmission is believed to be the primary

    route of infection, but bloodsucking p arasites like leeche s and the carp louse may serve a s mecha nicalvectors of SVCV. The g en ome of SVCV is composed of a single m olecule of line ar, nega tive-sen se,single-stranded RNA containing 5 gen es in the order 3-NPMGL-5 coding for the viral nucleopro-tein, ph osphoprotein, matrix protein, glycoprotein, and p olymera se, respectively. Polyacrylamide g elelectrophoresis of the viral proteins, and sequ ence homologies between the ge nes an d g ene junctionsof SVCV and vesicular stomatitis viruses, have led to the p laceme nt of the virus as a te ntative me mb erof the ge nus Vesiculovirusin the fam ily Rhabdoviridae. These me thods also revealed th at SVCV is notrelated to fish rha bdoviruses of the g enu s Novirha bdovirus. In vitroreplication of SVCV take s place inthe cytoplasm of cultured ce lls of fish, bird an d m am malian origin at tem pe rature s of 4 to 31C, with anoptimum of about 20C. Spring viremia of carp can be diagn osed b y clinical signs, isolation of virus in ce llculture an d molecular meth ods. Antibodies directed a ga inst SVCV react with the homologous virus inserum neutralization, immunofluorescence, immunoperoxidase, or enzyme-linked immunosorbentassays, but the y cross-react to various deg ree s with the p ike fry rhabd ovirus (PFR), sugge sting the 2viruses are closely related. However, SVCV and PFR can be distinguished by certain serologicaltests and molecular me thods such as the ribonuclease protection assay.

    KEY WORDS: Rha bd ovirus Spring viremia of carp virus SVCV Disease Cyp rinids Ca rp Fish d isease

    Resale or republication not permitted without written consent of the publisher

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    serious losses in carp pond fisheries of the centraland eastern p arts of Europe (Fijan 1972, 1999). Theassumed causes (nutrition, environment, parasites,ba cteria, viruses) for the a cute a nd chronic forms of theepizootics remained controversial for a long time.

    However, a viral etiology for the acute form of infec-tious dropsy became e vident w hen a cytopathic agen twas isolated (Osadchaya 1964, Toma $ec et al. 1964),and Rivers postulates were fulfilled using virus iso-lated from a ffected carp (Fijan et a l. 1971). In order todistinguish the viral disease from other aetiologicalen tities within the infectious dropsy complex, the dis-ea se wa s rena med spring viremia of carp (SVC), andthe ca usative virus was term ed spring viremia of carpviru s (SVCV) or Rhabdovirus carpio(Fijan et a l. 1971).The infectious disease of carp termed swim-bladderinflammation (SBI) was also recognized in Europe(Arshaniza et al. 1968, Otte 1972). A rhabdovirus iso-

    lated from ca rp e xhibiting the acute form of SBI (Ahne1973, Bachm ann & Ahne 1973, 1974) was found to beidentical to R. carpio(de Kinke lin & Le Berre 1974, Hillet al. 1975). Later, it was shown that the chronic dis-ease termed carp erythrodermatitis was caused by abacterium of the genus Aeromonas (Bootsma et al.1977). For more complete reviews of the history ofthe se con ditions, see Fijan (1999) or Wolf (1988).

    In Europe, SVCV mainly affects the common carpCyprinus carpio, but several other species of freshwater fishes can be infected (Fijan 1972, 1988, 1999,Wolf 1988). In carp, the most common external signsof SVC are hem orrhages of the skin, exopthalmia,

    abdominal distension, and an inflamed or e dema tous

    vent (Fig. 1A). Internal signs are peritonitis, ascites,catarrhal and hemorrhagic enteritis , edematous vis-cera and petechial hemorrhage s of the internal wall ofthe swimbladder and in skeletal muscle (Fijan et al.1971, Ahne & Wolf 1977, Ne ge le 1977).

    A rhabdovirus isolated from penaeid shrimps inHawaii (Lu et al. 1991) had a G gene that exhibitedover 99% identity to the G nucleotide sequence ofSVCV (Johnson et al. 1999). The agent caused histo-logical changes and significant mortality in penaeidshrimp s (Lu & Loh 1994). The SVCV-like virus isolatedfrom pena eid shrimp in H awaii was reported to causehistological changes and mortalities in Penaeusstylirostristhrough experimental water-born infection,oral feeding and intramuscular injection of the virus(Lu et al. 1991).

    Properties of SVCV

    SVCV exhibits the typical bullet-shaped morpho-logy of a vertebrate rhab dovirus (Wunne r et al . 1995)(Fig. 1B). The virion possesses a n inner nucleocap sidwith helical symmetry measuring about 50 nm in dia-meter. The virion me asures a pproximately 80 to 180 nmin length and 60 to 90 nm in d iameter. Truncated par-ticles, about 2/3 of the length of infective virions,repre sent defective, noninfectious virions (Fijan e t al.1971, Bachmann & Ahne 1973, Hill et al. 1975, Bishop& Smith 1977). SVCV has a buoyant density in CsClof 1.195 to 1.200 g cm 3 (Bachmann & Ahne 1973).

    Virus infectivity is destroyed at p H 3 an d 12, b y lipid

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    Fig. 1. Cyprinus carpio.(A) SVCV (spring viremia ofcarp virus)-infected com-mon carp showing petechialhemorrhages in the mus-cles, swim bladde r, enlargedspleen, edematous organsand pale gills with hemor-rhages. (B) Electron micro-graph of SVCV in infected

    fathead minnow (FHM) cellsshowing bullet-shape d par ti-cles. (C) Cytopathog enic ef-fect (CPE) of SVCV in FHMcells, 72 h after infection,20C. The C PE is character-ized by round ing of cells andfocal lysis of the monolayer(magnification: 200). (D)Detection of SVCV antigenin FHM cells, 24 h post injec-tion (p.i.) using indirect im-munofluorescence (magnifi-

    cation: 90)

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    solvents, and by heat (56C). The virus is inactivated

    within 10 min by formalin (3%), chlorine (500 ppm),iodine (0.01% ), Na OH (2% ), UV (254 nm) and g amm airradiation (103 krads). Freeze-thaw cycles partiallyinactivate the virus. During lyophilization, add ition of2 to 10% fetal calf serum protects the virus infectivity(de Kinke lin & Le Berr e 1974, Ahn e 1976, 1982).

    The virus is presen tly classified as a tenta tive m em-ber of the genus Vesiculovirusof the family Rhabdo-viridae(Walker e t al. 2000). As with other me mb ers ofthe genus, the virion of SVCV contains 5 structuralproteins (now te rmed N, P, M, G, L), the sizes of whichwere initially estimated by mobility in SDS-PAGE(sodium dodecyl sulphate polyacrylamide gel elec-

    trophoresis) gels (Lenoir 1973, Lenoir & deKinkelin 1975, Clerx & Horzinek 1978, Royet al. 1984). Recently, the availability ofsequen ce data for the entire SVCV genomeallows more accurate predictions of themolecular weigh ts of the structura l proteins(ignoring post-translational modifications)as we ll as other feature s of these m olecules(Table 1). The RNA-dependent RNA poly-mera se (L protein) functions in transcriptionand replication of the virus with an optimaltemperature for activity between 20 and

    25C (Roy & Clewle y 1978). Virus tran scrip-tion an d rep lication is achieved as the L pro-tein interacts with the P and N proteins ofthe nu cleocapsid. The glycoprotein (G pro-tein) of SVCV forms trimeric peplomers orspikes on the virus surface that bind to cel-lular receptors and induce viral end ocytosis.The surface glycoprotein acts as the mostimportant viral antigen that de termines theserological prop erties of rhab doviruses (Hillet al. 1975, Bishop & Smith 1977, Jrgensenet a l. 1989). The nucleoprote in (N prote in) is

    the most abun dant virion protein andinteracts with the viral RNA to formthe helical structure of the nucleo-capsid, and also has an important rolein modulating transcription. About 1/3

    of the N protein is associated withviral RNA (Sokol & Koprowski 1975).The phosphoprotein (P protein) is acomponent of the rhabd ovirus nu cleo-capsid that, in association with theL and N proteins , is required fortranscription (Wunner et al. 1975,Roy 1981). Like other ve siculoviruses,SVCV has one membrane protein(M protein). This basic protein formsthe bullet-shaped structure of thevirion and links the nucleocap sid w ith

    the cytoplasmic domains of the G protein embedded

    in the lipid-containing viral envelope (Walker et a l .2000) (Fig. 2).

    Genomic organization of SVCV

    The SVCV virion contains 1 molecule of linear,negative-sense, single-stranded RNA that sedimentsin 5 to 20% sucrose gradients at 38 to 40 S (Hill et a l.1975, Lenoir & de Kinkelin 1975, Clerx & Horzinek1978, Roy & Clew ley 1978, Wu et a l. 1987). Cha racte r-ization of this SVCV ge nomic RNA beg an in 1984 withpublications of the M g ene sequen ce and a 70 nucleo-

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    Table 1. Features of the 5 genes of the spring viremia of carp virus (SVCV)genome. N: nucleocapsid; P: phosphoprotein; M: matrix protein; G: glycopro-tein; L: polymerase. nt: nucleotides; aa: amino acids; mw: molecular weight;pI: isoelectric point. The last 3 columns refer to the protein pr edicted b y transla-tion of the open r ead ing frames (ORFs) in the n ucleotide sequ ence of the SVCVgen ome. Thus, the protein molecular weight is for the pre dicted product with no

    post-translational modification such as phosph orylation or glycosylation

    G e n e To ta l g e n e Upstream Dow nstre am O RF Prote in Prote in Prote inlength (nt) UTR (nt) UTR (nt) (nt) (aa) (mw) (p I)

    N 1335 10 68 1254 418 47000 5.57P 967 10 27 927 309 35622 4.46M 716 10 34 669 223 25627 8.61G 1588 10 48 1527 509 57338 5.54L 6325 10 (trailer) 6285 2095 238244 8.63

    L Polymerase

    G Glycoprotein

    N Nucleoprotein

    P Phosphoprotein

    M Matrix protein

    a) SVCV Virion

    G LN

    b) SVCV Genome RNA (11,019 nt)

    3 5MP

    Envelope

    c) conserved gene junction and upstream untranslated region:

    ...TATG(A) CTAACAGASATCATG...7

    Fig. 2. Spring viremia of carp virus (SVCV). (A) Virion structure, (B) ge-nomic organization, and (C) gen e junction sequen ces of SVCV

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    tide sequ en ce a t the 3 genom e term inus (Kiuchi & Roy1984, Roy et al. 1984). This line of investigation thenlays appa ren tly dorma nt until publication of the p artialL gene, complete G gene, and gene junction se-que nces in 1995 and 1996 (Bjorklund et a l. 1995, 1996).

    In 2001, 2 complete genomic RNA sequences of anAmerican type culture collection (ATCC) referencestrain of SVCV (VR-1390) were submitted to Gen-Bank by indepen dent laboratories (GenBank accessionU18101 by Bjorklund et al. 1996 and GenBank acces-sion AJ318079 by Hoffman et al.). With this da ta n owavailable, the genetic organization of SVCV can bedefinitively described. The genomic RNA is 11019bases in length. It contains 5 major open readingframes (ORFs), encoding predicted proteins homolo-gous to the 5 major structural proteins found in allrha bdoviruses. The ge nomic orde r is 3-NPMGL-5, asshown in Fig. 2B. This is identical to the g en etic orga-

    nization of species in the genera Vesiculovirus andLyssavirus. This confirmed ge ne order for SVCV clari-fies a ny confusion resulting from an ea rly pu blicationthat sugge sted an alternative organization (Wu e t al .1987). The SVCV genome does not have a non-virion(NV) gene between the G and L genes as is foundin fish rhabdoviruses of the ge nus Novirhabdovirus(Kurath et al. 1997, Walker et al. 2000). Similarly, itdoes not have a large non-coding region between theG a nd L gen e O RFs, as is found in lyssavirus ge nome s.Thus, the overall genome structure of SVCV is mostsimilar to that of the vesiculovirus g enu s.

    The SVCV genome has a 59 base putative leader

    region at the 3 terminus followed by a consensusstart signal (AACAG; mRNA-sense) for transcriptionof the N gene. Analysis of the SVCV N-gene mRNAby 5 RACE has confirmed that transcription starts atthis AACAG signal (W. Batts & G. Kurath unpubl.).The features of the 5 ge nes an d their protein productsare summarized in Table 1. Other than the 5 majorORFs, only one is longer than 50 amino acids in thestandard rhabdovirus orientation (53 amino acids,within the M gene), and there are several in thereverse orien tation, all less tha n 140 a mino a cids. It isnot known whether any of these small ORFs are

    expressed, and there is no indication of an over-lapping reading frame within the P gene encoding asmall basic protein, as has be en re ported for vesicularstomatitis New Jersey virus (VSNJV) (Spiropoulou &Nichol 1993).

    As described by Bjorklund et al. (1996), the 4SVCV gene junctions are str ictly conserved, with aTATG(A)7 tran scription stop/ polyaden ylation signa l atthe end of each gene, and an AACAG transcriptionstart signal for the following gene. The untranscribedinterge nic reg ions of SVCV are all dinucleotide s (CT),with the excep tion of the G -L ge ne junction which ha s

    a tetranucleotide (CTAT). These regulatory signalsand intergenic regions are highly conserved betweenSVCV and a ll vesiculoviruses, and the y differ fromthe gene junctions of viruses in other rhabdovirusgenera such as lyssaviruses or novirhabdoviruses.

    However, unlike other vesiculoviruses that have beencharacterized to date, the untranslated regions up-stream of all 5 SVCV genes are completely uniform,consisting of exactly 10 nucleotides preceding theATG-codon signa ling the start of translation (Table 1).The sequence of this 10-base region begins with therecognized vesiculovirus pentanucleotide transcrip-tion start signal and is highly conserved between thegene junctions: 4 of the SVCV genes (N, M, G, L)begin with the sequence AACAGACATC, and onlythe P ge ne has a single nucleotide difference mak ingit AACAGAGATC. Although the length of the up-stream untranslated regions is variable among other

    vesiculovirus genes, they begin with a consensussequence AACAGNNATC (Luis L. Rodriguez, USDAPlum Island Animal Disease Center, pers. comm.),which matches the conserved SVCV sequence at 8out of 10 sites. This identity at the 3 termini of thegene s provides confirmation for an early compa risonof transcript termini of SVCV and vesicular stomatitisIndiana virus (VSIV) that suggested conservation ofthe rhabdoviral genome sequences specifying the 5end s of transcript RNAs (Gupta et a l. 1979). The tran -scription stop/polyadenylation signal for the SVCV Lgene is followed by a 46 base trailer that forms the5 terminus of the gen ome.

    Sequen ce similarities betwee n SVCV and vesicularstomatitis viruses were first reported in 1984 usingcomplete M gene and 3 terminal genome sequences(Kiuchi & Roy 1984, Roy et al. 1984). The 3-terminal20 nucleotides we re found to be n early identical to thecorresponding sequences of both VSIV and VSNJV.Later, comparisons of the first 1780 amino acids of thepredicted SVCV L protein with partial L proteins ofother rhabdoviruses revealed closest homology withthe VSIV polymerase, although significant homologywas also found with the polymerase of rabies virus(Bjorklund et al. 1995). The homologies involved sev-

    eral highly conserved d omains separated by variableregions. The conserved domains most likely representpreviously identified RNA polymerase functional do-mains such as those for RNA binding, RNA templaterecogn ition, phosph odiester bond formation, and ribo-nucleotide triphosphate binding (Poch et al. 1990).There wa s very little similarity betwe en the L proteinsof SVCV and the novirhabdovirus, infectious hemato-poietic necrosis virus. The SVCV G gene encodes a509 amino acid protein with a predicted structuresimilar to othe r rh abd ovirus glycoproteins (Bjorklundet a l. 1996). It contains 2 m ajor hydroph obic doma ins

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    including the signal peptide and transmembrane do-main. The comp lete SVCV G prote in was most closelyrelated to members of the vesiculovirus genus, show-ing 31.2 to 33.2% amino acid identity (51.8 to 53.3%amino acid similarity) with VSIV, VSNJV, and chandi-

    pura virus (CHPV). In con trast, there wa s only 19.4 to24.3% amino acid identity (40.5 to 47.2% amino acidsimilarity) with G proteins of 11 rhabdoviruses fromother gen era.

    Phylogenetic analyses (Fig. 3) using the full-lengthamino acid sequences of the N, P, M, and G proteins,as well as partial sequences of the L proteins, con-firms the close relationship between SVCV and theestablished members of the Vesiculovirus genus(Bjorklund et al. 1996, Johansson 2001). Examples ofsuch phylogenetic trees are shown in Fig. 3 for full-length G and N p rotein seque nces. Despite minor dif-ferences in topology between the trees generated by

    the different genes, both indicate a close phylogenetic

    relationship be tween SVCV and accepted me mbers ofthe Vesiculovirus g enu s. This is supp orted by signifi-cant bootstrap values, providing a high level of con-fidence in this relationship. The 7th report of theInternational Committee for Virus Taxonomy lists

    SVCV as a tentative member of the vesiculovirusgenus (Walker et al. 2000). In the future, data includ-ing thorough phylogenetic analyses will be used insupport of a proposal that SVCV belongs within thisgenu s as a full member, as has bee n sugge sted previ-ously (Bjorklund et a l. 1996).

    Within the species SVCV, the genetic diversityamong SVCV strains has been demonstrated by bio-logical and serological ana lyses (Jrgen sen e t al. 1989)and by ribonuclease protection assays (Ahne et al.1998). Although there are not yet any published re-ports characterizing seque nce diversity be tween strains,this is an are a of active investigation in several labora-

    tories.

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    Fig. 3. Phylogenetic relationships of (A) nucleocapsid and (B) glycoprotein ge ne sequ ence s of spring viremia of carp virus (SVCV)and 15 other rha bdoviruses. The viral species and the GenBank sources for their N a nd G amino acid sequences w ere: SVCV(U18101); vesicular stomatitis New Jersey virus (VSNJV, K02379, J02433); vesicular stomatitis Indiana virus (VSIV, J02428);

    Cha ndipu ra virus (CHPV, M16608, J04350); viral hemorr hag ic septicemia virus, strain 0771 (VHSV-0771, AJ233396); viral hem-orrhag ic septicemia virus, strain Ma kah (VHSV-Mak , X59241, U28747); infectious hem atopoietic necr osis virus (IHNV, L40883);Hirame rhabdovirus (HIRRV, AF104985, U24073); snakehead rhabdovirus (SHRV, AF147498); Rabies virus, Pasteur vaccinestrain (RABPV, M13215); Mokola viru s (MOKV, Y09762, S59447); Adela ide River viru s (ARV, U10363, L09207); bovine e ph em era lfever virus (BEFV, AF234533); Sigma virus (SIGMA, X91062); lettuce necrotic yellows virus (LNYV, L30103, AJ251533); andsonchus yellow net virus (SYNV, L32603). Sequences were aligned using Clustal X (Thompson et al. 1997) and analyzed withPAUP* 4.0 (Swofford 2000) neighbor-joining (shown) and parsimony ph ylogen y program s (not shown). Sequen ces from the p lantrhab dovirus SYNV wer e used to outgroup the a nalyses. Each tree rep resen ts the consensus of 1000 bootstrappe d rep licates of thedata , with bootstrap confiden ce values along the bran ches to indicate the p erce nt of 1000 trees tha t contained exactly the group-ing shown to the right of the value . Branche s with bootstrap value s less than 70 we re collapsed to avoid suggesting un certain re -lationships. The viral species included represent the 6 accepted rhabdovirus genera and one un assigned species (Sigma virus).Genera are indicated by brackets labeled as follows: V, Vesiculovirus; N , Novirhabdovirus; L, Lyssavirus; E, Ephemerovirus; C ,Cytorhabdovirus; Nu, Nucleorhabdovirus. Note that the position of SVCV (in bold and asterisked) relative to the 3 acceptedmembers of the Vesiculovirus genus (VSNJV, VSIV, and CHPV) suggests that SVCV should be included in this genus

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    In vitromultiplication of SVCV

    SVCV rep licates in ce ll cultures originated from fish,birds and ma mmals betwee n 4 an d 31C (Ahne 1973,Clark & Soriano 1974). Cytopathic effects (CPE), like

    marg ination of nuclear chromatin followed b y roundingup an d lysis of cells (Fig. 1C), ap pe ar at va rying time s ofinfection dep end ing on the tem perature and cell l inesused. The optimal temperature of viral replication invitrois betwee n 20 an d 25C. The be st cell systems formultiplication of SVCV a re th ose de rived from cyprinidfishes (e.g. primary cell cultures or established cellline s) such as the epithelioma papillosum cyprini(EPC)cell line (Fijan e t al. 1983), the fathead minnow (FHM )cell line (ATCC CCL-42, Gravell & Malsberger 1965),and carp leuk ocyte cultures (CLC, Europe an Collectionof Cell Culture s 95070628, Faisal & Ahn e 1990). Usingthese cell lines, infectivity titers of about 108 TCID50

    ml1 were obtained regularly. Actinomycin D does notaffect SVCV re plication (de Kinke lin & Le Berr e 1974).The virus forms well-defined plaques in permissivecells 72 h after infection. A single step growth curvecarried out in FHM cells at 20C showed that the firstprogeny virus is synthesized 4 to 6 h after infection.Both cell-associated and cell-free virus reach peaktiters betwe en 10 an d 22 h after infection. One g rowthcycle of the virus lasts 8 to 10 h at 20C (Ahne 1973,Bachmann & Ahne 1974). SVCV also replicates inchicken embryo fibroblasts, in mammalian cells suchas BHK 21 (hamster), fetal calf kidney (cattle), HEP-2(hum an ), MDC K (canine ), SK (porcine), Vero (monk ey)

    an d in several reptilian ce ll lines, provided tha t incub a-tion temperatures be tween 20 and 22C are used (Ahne1973, Bach ma nn & Ahn e 1974, Clark & Soriano 1974). Ithas been demonstrated that apoptosis is involved indeath of EPC cells caused by SVCV (Bjorklund et al.1997). Morphological changes, like reduction of cellvolume, blebbing, and formation of apoptotic bodies,appear 36 h after infection of cells. About 40 h later,more than 70% of the SVCV-infected EPC cells werefound to be a poptotic. It is likely that th e pr ogramm edcell death of the SVCV-infected cells depends onrep lication and produ ction of progen y virus. Apoptosis

    could be inhibited by the endogenous acid cysteineproteinase inhibitor, cystatin A, which has been puri-fied from h um an p alatine tonsils (Bjorklund e t al. 1997).Experiments showed tha t SVCV-indu ced ap optosis canalso be inh ibited by z-VAD-fmk, an inhibitor of caspa se1, 3, 4 and 7 (Tae htinen et a l. 1999).

    Antigenic properties of SVCV

    Several studies showed that carp de velop a humoralimmune response to SVCV (Sulimanovic 1973, Klbl

    1975, Fijan et a l. 1977a,b, Baudouy 1978, Ahne 1980,Baudouy et al. 1980a,b, Fijan & Mata $in 1980, Fijan1988). Rha bd ovirus-neutralizing a ntibodies are d irectedagainst the surface glycoprotein of the virus (Kellyet al. 1972). Induction of hum oral an tibodies aga inst

    SVCV in carp is influe nced by the a ge a nd cond ition ofcarp, by the route of infection and, most importantly,by the temperature of water (Fig. 4). In carp whichwere infected by waterborne e xposure to low doses ofSVCV and k ept a t 20C, SVCV neutralizing a ntibodiesapp ea red 7 d a fter infection. In contrast, carp infectedin the same way, but kept at 13C, showed first de-tectable an tibodies 7 wk after infection. At 13C, carpdeveloped a subclinical infection with presence ofvirus in th e b lood of carp for about 10 w k. Ne utralizingantibodies which appeared 8 to 10 wk after infectionlead to a rapid decline of the amount of virus in theblood (Ahne 1979, 1980, 1986). The biological proper-

    ties of the SVCV ne utralizing a ntibodies have not bee nstudied in detail, but prob ably resemb le the tetram ericantibody typically found in teleost fishes (Fijan et al.1977a, Kaa ttari & Pigan elli 1996).

    Cross-neutralization studies using the fish rhabdo-viruses, infectious h em atop oietic necrosis virus (IHNV),viral hemorrhagic septicemia virus (VHSV), hiramerhabdovirus (HIRRV) and their respective antisera,revealed no antigenic relationships between SVCVand these members of the Novirhabdovirus genus ofth e Rhabdoviridae (de Kinkelin & Le Berre 1974, deKinkelin et al. 1974, Hill et al. 1975). However, sero-logical examination of 22 rhabdovirus isolates from

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    Fig. 4. Influence of water temperature on SVCV (springviremia of carp virus)-infection of ca rp Cyprinus carpiolead-ing to virus m ultiplication (10 to 12C) or to prod uction of ant i-bodies (20 to 22C). SPF carp (25 to 30 g) were intraperi-toneally infected with 103 TCID50 of SVCV. Infected fish kep tat 10 to 12C and 20 to 22C were analyzed for values of

    virus, antibodies an d dea th (Ahne 1980)

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    Cyprinidae, Esocidae and Siluridae genera indicatesclose relationship between SVCV and the vesiculo-virus-like fish rh ab dovirus, pike fry rhab dovirus (PFR,Jrgensen et al. 1989). These authors showed thatSVCV and PFR cross-reacted by indirect immuno-

    fluorescence (Fig. 1D) using polyclonal antisera andshared common antigenic determinants on the G, Nand M proteins as revealed by immun oblotting. The 2viruses could, however, be differentiated by neutral-ization assays using certain polyclonal antisera in theabsence of complement. Consequently, it was sug-gested that SVCV and PFR should be considered asrepresentatives of 2 serotypes of 1 virus species (Jr-gensen et al. 1989). The 2 viruses could also bedifferentiated by a ribonuclease protection assayusing a probe ma de from transcripts of the G geneof SVCV (Ahne et al. 1998), indicating thatgenetic differences exist between the 2 viruses.

    Resolution of the b iological and gen etic relation-ships between isolates of SVCV and PFR is im-portant because isolation of SVCV from fish isnotifiable to the Office International des Epi-zooties (OIE) wh ile PFR is not.

    Experimental infection of carp with SVCV

    The systemic character of SVCV infection hasbeen demonstrated by experimental infection ofspecific pathogen free (SPF) carp (Ahne 1977,1978). Following waterborne infection of carp at

    13C, the virus was initially detecte d in the gills,suggesting they were the first targeted organ.Following an eclipse-like pe riod of 4 d, SVCV wa ssprea d via blood to the interna l orga ns of infectedfish. Eleven days after infection, SVCV wasexcreted from the alimentary tract in the fecesand mucous casts. First mortality due to SVCVinfection app ea red 20 d after infection. The incu-bation period of the water borne SVCV infectionwas found to be 7 d un der the e xperimen tal con-ditions used (Fig. 5). First clinical signs such asede ma tous viscera, peritonitis, enteritis and he m-

    orrhages in different organs could be recognized8 to 11 d after infection. The virus persisted ininfected carp for more than 10 wk and those fishbecame SVCV carriers (Ahne 1977, 1978, 1980).

    Histopathology of SVC

    Precise reports on histological changes ofSVCV-infected carp a re rare . The following histo-logical findings have been obtained in experi-men tally infected carp fingerling s (Ne ge le 1977).

    The ra nge of alterations of the liver wen t from pe rivas-culitis showing lymphocytes and histiocytes infiltra-tion, to panvasculitis with a high grade of edematiza-tion and a concurrent loss of structure of blood vesselwalls. The blood vessels appeared to be fully necrotic

    in the final stage of the disease. The liver pa rench ymashowed multifocal necroses, adipose de gen eration a ndhyperemia. In the pancreas, non-purulent inflamma-tion and multifocal necrobiosis were usually seen. Inthe parietal and visceral serosa of the peritoneum,peritonitis was predominant. Lymph vessels wereextremely dilated and filled up with detritus, macro-ph age s, and lymphocytes. In the intestine, perivascular

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    PFU ml1 (g tissue)

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    virus amountin the water

    virusamountin feces

    Fig. 5. Spread of spring viremia of carp virus (SVCV) through thebody of carp Cyprinus carpioafter waterborne infection for 2 h at13C. SPF (specific pathoge n free ) carp (25 to 30 g) were intraperi-toneally infected with 104.4 plaqu e-forming un its (PFU) ml1 of SVCVby wate rbath a t 13C. Two hours after infection, SVCV was detecte donly in the gills. After a 4 d eclipse period, progeny viruses weredessimated to internal organs via the bloodstream. Two viremiastages were recognized 6 and 10 d after infection. The incubation

    period lasted 7 d at 13C (Ahne 1978)

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    inflammation and desquamation of epithelium with asubsequent atrophy of the villi have been often recog-nized. The spleen was hyperemic and showed a con-siderable hyperplasia of the reticuloendothelium.Siderocytes and cells with increase d lipofuscin storage

    were present. The tubuli of the kidne y were cloggedby the tube casts, and vacuolation and hyaline d egen -eration were p resen t. The lamina ep ithelia of the swimbladder cha nged into a discontinuous m ultilayer andin the submucosa dilated vessels and hemorrhageswere evident. The hea rt showed discontinuous myode-generation and inflammatory alterations of the peri-cardium.

    Natural outbreaks of SVC

    SVC is reported to be present in several European

    countries (Austria, Bulgaria, France, Germany, GreatBritain, Hungary, Italy, Spain, as well as in parts of theformer C zechoslovakia, Soviet Union an d Yugoslavia;Toma$ec et al. 1964, Fijan et al. 1971, Ghittino et al.1971, Ahne 1973, Baudouy 1975, Klbl 1975, Tesar

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    the spring. The behavior and external signs in easilycaught moribund fish exhibiting hem orrhages in skin,pale gills, ascites, etc., warrant necropsy and furthersamp ling of fish for virological exa mination. Presum p-tive diagnosis is based on the presence of enteritis,

    peritonitis, edema, petechial bleedings in the swimbladd er, muscles and other organ s. Lack of some signsor their slight pronouncemen t do not exclude the needfor laboratory exam ination. Variations and differe ncesof disease signs in a population should be encom-passed by a selection of separate samples, and allaffected species should be sa mpled . Whole fishes nea rdeath or freshly dead specimens should b e chilled andimmediately delivered to a specialized or authorizedlaboratory.

    Spring viremia of carp is listed a s a n otifiable d isea seby the (see www.oie.int). Diagnostic proceduresshould be b ased on th e OIE guidelines (Office Intern a-

    tional des Epizooties 2000). Etiological diagnosis ofSVC is secure d b y the p roof of virus presen ce in tissuesamp le using electron m icroscopical techn iques, cryo-stat thin section immunofluorescence, or isolation ofthe a ge nt. For the latter, cell lines such a s FHM or EPCare recommended by the OIE. Cell monolayers areinoculated with 10-fold dilutions of homogenates ofkidney, spleen, liver and encephalon. Infected cellcultures incubated at 20C usually show cytopatho-genic effects after 24 to 48 h. The virus yield in theinternal organs can vary between 104 to 107 TCID50ml1 , depen ding on the ph ase of disease de velopmen t.The isolated virus can be identified by serological

    techniques such as the serum neutralization test (NT),immunofluorescence (IF), immunoperoxidase (IP), orenzyme linked immunosorbent assay (ELISA) (Ahne1981, Faisal & Ahne 1984, Jrgensen et al. 1989,Way 1991, Rodak et al. 1993), although the an tiserumused must be of high quality (Dixon & Hill 1984). Inroutine diagnostics, immunohistological techniquesusing virus-infected cell culture s or a cryostat thin sec-tion of infected organs are generally considered to bethe most reliable and convenient techniques for virusidentification. Fundamental reagents are standardantige n (SVCV re ference strain ATCC VR-1390, Fijan

    et a l. 1971) an d p olyclona l, or pre ferably monoclonal,antibodies (BIO-FLOU SVC, Bio-X, 30 Hoogveldiaan,1700 Dilbe ek , Belgium ). SVCV is serologically distinctfrom the other known fish rhabdoviruses, with theexception of PFR that cross-reacts with SVCV byimmunofluorescence and ELISA (Jrgensen et al.1989, Way 1991). The indirect diagnosis of SVCV isbased on detection of virus-specific antibodies in thefish serum. For seroepidemiological surveys, NT, IF orELISA are usua lly used . The immu ne status of investi-gated fish revealed a high incidence of serologicallypositive carp farms in Europ e (Ahne 1979, Dixon e t al.

    1994). As alread y described a bove, SVCV shares a nti-genic determinants with PFR (Jrgensen et al. 1989,Way 1991). SVCV and PFR cannot be reliably distin-guished by certain serological approaches, especiallyIF and ELISA. Both rhabdoviruses are listed as tenta-

    tive species in the genus Vesiculovirus of the Rhab-doviridae(Walke r et a l. 2000), bu t PFR is, in contra st toSVC, not an OIE notifiable agent. Therefore, propermethods should be used to distinguish between iso-lates of SVCV and PFR. A ribonuclease protectionassay (RPA) was developed that can distinguish be-tween SVCV and PFR (Ahne et al. 1998). Probes forthe full- leng th G gene of SVCV were used successfullyto discriminate 13 viruses from different teleost fishescross-reacting in the SVCV/PFR-IF. In addition, RPAresults revealed genetic diversity among SVCV iso-lates obtained from differe nt carp spe cies and differe ntlocations. Molecular methods for detection of SVCV

    are not widely used at present and are not includedamong the a pproved m ethods of the O IE. However, asemi-nested PCR has been established to identify theSVCV G gene in fish tissues (Liu et al. 1998). Thiscould be a method to screen for SVCV in chronic orpe rsistently infected fish or in fish tha t are carriers ofthe virus. As RNA viruses usually form quasi-speciesthat include wide g enomic variation, some g enotypeswill only have a selective advantage if growth condi-tions change (Steinhauer & Holland 1987). Ore shkovaet al. (1995, 1999) used the reverse transcriptasePCR (RT-PCR) developed for the M a nd G gene andhybridization with non-radioactive probes for detec-

    tion of SVCV. Biotinylated probes used for hybridiza-tion were 248 bp fragments of the M gene. Dot blotsga ve se nsitive virus spe cific signa ls in tissue sa mplesof experimentally infected carp fingerlings if thevirus titers were ap proximately 105 TCID50 g tissue

    1 .Reage nts for SVCV diagn osis can be ob tained from theOIE referen ce lab oratory for SVCV.1

    Prophylaxis and control of SVC

    Temperatures above 20C usually secure in carp a

    level of meta bolic activity that e na bles produ ction of pro-tective levels of inte rferon (Baudoy 1978) and antibodies(Ahne 1980). There fore, SVC-diseased fish h ave so farnot bee n rep orted in tropical an d subtrop ical clima tes. Inrea ring facilities with a controlled en vironme nt, eleva-tion of tempe rature can prevent or stop SVC outbreaks.In tem perate climates, avoidance a nd eradication seem

    9

    1The Centre for Environment, Fisheries & Aquaculture Sci-ences, Weymouth Laboratory, Barrack Road, The Nothe,Weymou th, Dorse t DT4 8UB, UK ([email protected] k).

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    possible on modern small farms using spring or wellwater. On large carp farms, gen eral prevention and con-trol measures have little chance of being effective.Location on , an d conne ctions with, large surface wa tersystems make it impossible to prevent natural move-

    men ts of carriers such a s carp and pe rhap s other fishe sfrom farms to open waters and back. Selection, hy-bridization and genetic manipulation of carp for SVCresistance has n ot yet resulted in a tested and acceptedstrain. This approach to preven tion h as a long trad ition inRussia. Kirpichnikov et al. (1987) reported results ofstrain selection, an d Wolf (1988) men tione d th e highlytouted resistance of the Krasnodar strain, but data oncontrolled challenge s of such carp strains are still lack-ing. Effective a nd safe immunoproph ylaxis has not be enestablished yet. However, carp vaccinated intraperi-tonea lly or orally in autu mn w ith live virus can de velop asolid resistance to reinfection, which can last several

    months including overwintering (Fijan et al. 1977a,b,Fijan 1988, 1999). A commercial inactivated SVCVpreparation for intraperitoneal delivery gave positiveresults in vaccinations of carp in Eastern Europe(Tesar

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    Bjorklund H V, Higman KH, Kurath G (1996) The g lycoproteingenes and gene junctions of the fish rhabdoviruses springviremia of carp virus and hirame rhabdovirus: analysis ofrelationships with other rhab doviruses. Virus Res 42:6580

    Bjorklund HV, Johansson TR, Rinne A (1997) Rhabdovirus-induced apoptosis in a fish cell line is inhibited by a

    human endogenous acid cysteine proteinase inhibitor.J Virol 71:56585662Bootsma R, Fijan N, Blommaert J (1977) Isolation a nd pre lim-

    inary identification of the ca usative ag ent of carp e rythro-dermatitis. Vet Arh 47:291301

    Bucke D, Finlay J (1979) Identification of spring viremia incarp (Cyprinus carpio) in Grea t Britain. Vet Rec 169:6971

    Bussereau F, de Kinkelin P, Le Berre M (1975) Infectivity offish rhabdoviruses for Drosophila melanogaster. An nMicrobiol (Paris) 126A:389 395

    Clark HF, Soriano EZ (1974) Fish rhabdovirus replication innon-piscine cell culture: new system for the study of rhab-dovirus-cell interaction in which the virus and cell havedifferent temperature optima. Infect Immu n 10:180188

    Clerx JPM, Horzinek MC (1978) Comparative protein ana-lysis of non-salmonid fish rhabdoviruses. J Gen Virol 40:

    287295Corbeil S, La Patra SE, Anderson ED, Kurath G (2000) Nano-

    gram q uan tities of a DNA vaccine to protect rainbow troutfry against heterologous strains of infectious hematopoi-etic necrosis virus. Vaccine 18:28172824

    de Kinke lin P, Le Berr e M (1974) Rhab doviru s des poisson s. II.Proprietes in vitro du virus printaniere de la carpe. AnnMicrob iol (Paris) 125A:113124

    de Kinke lin P, Le Berre M, Lenoir G (1974) Rhab dovirus despoissons. I. Proprietes in vitro du virus de la ma ladie rougede lalvin de broch et. Ann Microbiol (Paris) 125A:93111

    Dixon PF, Hill BJ (1984) Rapid d ete ction of fish rha bd oviruse sby the enzyme-linked immunosorbent assay (ELISA).Aquaculture 42:112

    Dixon PF, Hattenberger-Baudouy AM, Way K (1994) Detec-tion of carp a ntibodies to spring viraemia of carp virus b ya comp etitive immu noassay. Dis Aqua t Org 19:181186

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