Cookies on Invasive Species Compendium

Like most websites we use cookies. This is to ensure that we give you the best experience possible.

 

Continuing to use www.cabi.org  means you agree to our use of cookies. If you would like to, you can learn more about the cookies we use.

Datasheet

koi herpesvirus disease

Summary

  • Last modified
  • 27 July 2017
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • koi herpesvirus disease
  • Pathogens
  • koi herpesvirus
  • Overview
  • Koi herpesvirus disease (KHVD) is a disease of common carp, Cyprinus carpio, and its ornamental varieties that has had a significant effect on their culture since the mid- to late-1990s. The disease, as far as is...

Don't need the entire report?

Generate a print friendly version containing only the sections you need.

Generate report

Pictures

Top of page
PictureTitleCaptionCopyright
koi herpesvirus disease; symptoms. An example of gill damage in a KHV infected carp (a); carp with a sunken eye (b); normal fish (c). UK.
TitleSymptoms
Captionkoi herpesvirus disease; symptoms. An example of gill damage in a KHV infected carp (a); carp with a sunken eye (b); normal fish (c). UK.
Copyright©Open Government Licence/https://www.nationalarchives.gov.uk/doc/open-government-licence/version/1/
koi herpesvirus disease; symptoms. An example of gill damage in a KHV infected carp (a); carp with a sunken eye (b); normal fish (c). UK.
Symptomskoi herpesvirus disease; symptoms. An example of gill damage in a KHV infected carp (a); carp with a sunken eye (b); normal fish (c). UK.©Open Government Licence/https://www.nationalarchives.gov.uk/doc/open-government-licence/version/1/
koi herpesvirus disease; dead fish in a lake. Clinical signs of KHV can include: Lethargy, 'hanging' in the water, gathering at water inlets or points of aeration. Although such fish superficially appear similar to basking fish, sick fish won’t 'spook' away as vigorously as a healthy fish, if at all. Damaged gills, with patches of pale, dead or rotting tissue. The eyes can appear sunken. The mucus covering the skin can appear as if flaking off, making the fish feel dry and rough when handled. There may also be secondary infections caused by parasitic, fungal or bacterial pathogens.
TitleMortality
Captionkoi herpesvirus disease; dead fish in a lake. Clinical signs of KHV can include: Lethargy, 'hanging' in the water, gathering at water inlets or points of aeration. Although such fish superficially appear similar to basking fish, sick fish won’t 'spook' away as vigorously as a healthy fish, if at all. Damaged gills, with patches of pale, dead or rotting tissue. The eyes can appear sunken. The mucus covering the skin can appear as if flaking off, making the fish feel dry and rough when handled. There may also be secondary infections caused by parasitic, fungal or bacterial pathogens.
Copyright©Open Government Licence/https://www.nationalarchives.gov.uk/doc/open-government-licence/version/1/
koi herpesvirus disease; dead fish in a lake. Clinical signs of KHV can include: Lethargy, 'hanging' in the water, gathering at water inlets or points of aeration. Although such fish superficially appear similar to basking fish, sick fish won’t 'spook' away as vigorously as a healthy fish, if at all. Damaged gills, with patches of pale, dead or rotting tissue. The eyes can appear sunken. The mucus covering the skin can appear as if flaking off, making the fish feel dry and rough when handled. There may also be secondary infections caused by parasitic, fungal or bacterial pathogens.
Mortalitykoi herpesvirus disease; dead fish in a lake. Clinical signs of KHV can include: Lethargy, 'hanging' in the water, gathering at water inlets or points of aeration. Although such fish superficially appear similar to basking fish, sick fish won’t 'spook' away as vigorously as a healthy fish, if at all. Damaged gills, with patches of pale, dead or rotting tissue. The eyes can appear sunken. The mucus covering the skin can appear as if flaking off, making the fish feel dry and rough when handled. There may also be secondary infections caused by parasitic, fungal or bacterial pathogens.©Open Government Licence/https://www.nationalarchives.gov.uk/doc/open-government-licence/version/1/

Identity

Top of page

Preferred Scientific Name

  • koi herpesvirus disease

International Common Names

  • English: carp nephritis and gill necrosis virus disease; koi herpesvirus infection

English acronym

  • CNGV disease
  • KHVD

Pathogen/s

Top of page koi herpesvirus

Overview

Top of page

Koi herpesvirus disease (KHVD) is a disease of common carp, Cyprinus carpio, and its ornamental varieties that has had a significant effect on their culture since the mid- to late-1990s. The disease, as far as is known, only affects C. carpio, but the causative virus is highly infectious for that species and is easily transmitted to susceptible individuals or populations. The disease appears to have been spread to most continents with the transfer of ornamental carp, and in many countries has then been transmitted to common carp, both cultivated and feral. The causative virus is believed to be a herpesvirus, koi herpesvirus (KHV), by many research groups, but other groups believe that the evidence for the virus to be a herpesvirus is lacking, and have named the virus carp nephritis and gill necrosis virus (CNGV) after some of the main pathological features of the disease. The taxonomic status of the virus will be resolved by further research. The virus can be isolated in cell culture, but isolation from infected fish is not consistent. However, molecular diagnostic methods are more reliable. There is a need for more sensitive cell cultures, and for the different molecular diagnostic methods to be compared so that sensitive, standardized methods can be used for diagnosis. Vaccination protocols are being developed, and there is a need for further research in that area, particularly with regard to the safety of live virus vaccines, and the need to distinguish between vaccinated fish and fish naturally infected with the virus during health screening programmes. More research is needed on the virus carrier state.

Hosts/Species Affected

Top of page

The disease occurs in common carp (Cyprinus carpio) and its ornamental varieties, such as the koi carp; the common and koi carp are sometimes distinguished as C. carpio carpio and C. carpio koi respectively. The disease occurs at temperatures between 16 and 25°C (Walster, 1999, 2003; Hedrick et al., 2000; Denham, 2003; Perelberg et al., 2003; Sano et al., 2004a,b; Terhune et al., 2004; Tu et al., 2004a). Experimental infections have been successful at 28°C (Gilad et al., 2004) producing 85% mortality, but at 29 or 30°C no mortalities occurred over 22- to 25-day periods (Hutoran et al., 2005; Perelberg et al., 2005). Under experimental conditions, 90.5-100% of bath-infected fish died at 23°C, 89.4-95.2% of fish died at 18°C, but no mortalities occurred at 13°C (Gilad et al., 2004). Viral DNA was detected in those fish by the polymerase chain reaction (PCR), which led the authors to suggest that infected fish that were surviving at lower temperatures may act as reservoirs for the virus. Transmission of the disease occurs following cohabitation of naïve fish with susceptible fish. Under natural conditions koi carp between 8-67 cm are susceptible (Bretzinger et al., 1999) as are common carp between approximately 500 g to 2 kg (Sano et al., 2004a,b; Terhune et al., 2004). Perelberg et al. (2003) reported that under experimental conditions young fish (2.5-6 g) were more susceptible than older fish (230 g).

Other species such as goldfish, Carrassius auratus, Nile tilapia (Oreochromis niloticus), silver perch (Bidyanus bidyanus), silver carp (Hypophthalmichthys molitrix), grass carp (Ctenopharyngodon idellus), sturgeon (Acipenser sp.) giant gouramy (Osphronemus goramy), Indonesian catfish (species unknown) and Siamese catfish (Pseudomystus siamensis), have been cultured with koi or common carp suffering from KHVD, but no mortalities or signs of disease were observed (Bretzinger et al., 1999; Hedrick et al., 2000; Denham, 2003; Perelberg et al., 2003; Sunarto et al., 2004). The former five species that were then cohabited with naïve carp did not transmit the disease (Perelberg et al., 2003). Goldfish, grass carp, golden shiners (Notemigonus crysoleucas) and fathead minnows (Pimephales promelas) are not susceptible to experimental infection with the virus (Goodwin, 2000; Hedrick et al., 2000).

Distribution

Top of page

The disease was initially reported from Israel and European countries in the late 1990s, but since then has spread to, or has been recognized in, a number of countries throughout the world. In many instances the disease was first reported before there was a method available, such as the polymerase chain reaction (PCR), to identify the aetiological agent, but subsequently the disease has been confirmed as Koi herpesvirus (KHV). The following are countries in which KHV has been identified: Austria, Belgium, China (Hong Kong), Denmark, France (Haenen et al., 2004), Germany (Bretzinger et al., 1999), Indonesia (Sunarto et al., 2004) Israel (Hedrick et al., 2000; Perelberg et al., 2003), Japan (Sano et al., 2004a,b), Luxembourg, (Haenen et al., 2004), Malaysia (Gilad et al., 2003; in fish imported into the UK, Haenen et al., 2004; Musa et al., 2005), The Netherlands, Poland (Haenen et al., 2004), South Africa (Haenen et al., 2004; McVeigh, 2004), Switzerland (Haenen et al., 2004), Taiwan (Tu et al., 2004a,b), Thailand (in fish imported into Germany, Haenen et al., 2004), UK (Walster, 1999, 2000; Denham 2003), and the USA (Hedrick et al., 2000). Histopathology and electron microscopy suggest that KHVD is present in Italy, but this has not been confirmed by the PCR (Haenen et al., 2004). Surveys for the virus are being conducted in Thailand by virus isolation and/or PCR, but to date are negative for the virus (Kanchanakhan, 2004), although fish originating from that country were positive for the viral DNA by PCR (referenced above). The stress of transportation may have activated a latent infection in the fish, facilitating identification of the virus/viral DNA. The disease was first detected in Japan in 2003, and by May of 2004 had spread to 24 out of 47 prefectures (Sano 2004b); by mid June of 2004 it had spread to a further 14 prefectures (Haenen et al., 2004). Analysis of archive histological material by in situ hybridisation has shown that KHV DNA was present in koi and common carp tissues taken during an unexplained mass mortality in 1996 in the UK (Haenen et al., 2004). The disease may have been present in South Africa since 2002 (McVeigh, 2004).

The presence of KHV in Korea is uncertain. Oh et al. (2001) described a disease in carp that had been occurring since 1998 and had affected more than 70% of carp farms. Seven farms surveyed had mortalities between 60-95%, and nationally, the disease had caused a drop in carp production. Some of the clinical signs were the same as those observed in KHVD, but the supposed causative virus that was isolated in fathead minnow (FHM) cells, was 70-80 nm dia and morphologically unlike a herpesvirus. Those two factors suggest that the virus was not KHV. However, Choi et al. (2004) observed a herpes-like virus in spleen tissues from carp in Korea that had many of the clinical signs of KHV disease. The virus needs to be identified by PCR. Clinical signs of KHV have been observed in carp in lake and pond culture systems in Lao PDR (Theungphachanh, 2004).

Distribution Table

Top 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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanNo information availableOIE, 2009
ArmeniaDisease never reportedOIE, 2009
AzerbaijanDisease never reportedOIE, 2009
BahrainDisease never reportedOIE, 2009
BangladeshDisease never reportedOIE, 2009
BhutanNo information availableOIE, 2009
CambodiaNo information availableOIE, 2009
ChinaDisease never reportedNULLHaenen et al., 2004; Sunarto et al., 2004; OIE, 2009
-Hong KongPresentOIE, 2009
IndiaNo information availableOIE, 2009
IndonesiaNo information availableOIE, 2009
-JavaPresentSunarto et al., 2004
-KalimantanPresentSunarto et al., 2004
-Nusa TenggaraPresentHaenen et al., 2004
-SulawesiPresentSunarto et al., 2004
-SumatraPresentSunarto et al., 2004
IranDisease never reportedOIE, 2009
IraqNo information availableOIE, 2009
IsraelPresentNULLHedrick et al., 2000; Perelberg et al., 2003; OIE, 2009
JapanPresentNULLSano et al., 2004a; Sano et al., 2004b; OIE, 2009
JordanNo information availableOIE, 2009
KazakhstanNo information availableOIE, 2009
Korea, Republic ofNo information availableNULLChoi et al., 2004; OIE, 2009
KuwaitNo information availableOIE, 2009
KyrgyzstanNo information availableOIE, 2009
LaosNo information availableNULLTheungphachanh, 2004; OIE, 2009
LebanonNo information availableOIE, 2009
MalaysiaPresentNULLGilad et al., 2003; Haenen et al., 2004; OIE, 2009
-Peninsular MalaysiaPresentMusa et al., 2005
MongoliaNo information availableOIE, 2009
MyanmarNo information availableOIE, 2009
NepalNo information availableOIE, 2009
OmanNo information availableOIE, 2009
PakistanNo information availableOIE, 2009
PhilippinesNo information availableOIE, 2009
QatarNo information availableOIE, 2009
Saudi ArabiaNo information availableOIE, 2009
SingaporePresentOIE, 2009; OIE, 2009
SingaporeDisease not reportedOIE, 2009; OIE, 2009
Sri LankaNo information availableOIE, 2009
SyriaNo information availableOIE, 2009
TaiwanPresentTu et al., 2004a; Tu et al., 2004b
TajikistanNo information availableOIE, 2009
ThailandNo information availableNULLHaenen et al., 2004; OIE, 2009
TurkeyNo information availableOIE, 2009
United Arab EmiratesNo information availableOIE, 2009
VietnamNo information availableOIE, 2009
YemenNo information availableOIE, 2009

Africa

AlgeriaNo information availableOIE, 2009
AngolaNo information availableOIE, 2009
BeninNo information availableOIE, 2009
BotswanaNo information availableOIE, 2009
Burkina FasoNo information availableOIE, 2009
ChadNo information availableOIE, 2009
CongoNo information availableOIE, 2009
DjiboutiNo information availableOIE, 2009
EgyptNo information availableOIE, 2009
EritreaNo information availableOIE, 2009
EthiopiaNo information availableOIE, 2009
GambiaNo information availableOIE, 2009
GhanaNo information availableOIE, 2009
GuineaNo information availableOIE, 2009
Guinea-BissauNo information availableOIE, 2009
KenyaNo information availableOIE, 2009
LesothoDisease never reportedOIE, 2009
MadagascarNo information availableOIE, 2009
MalawiNo information availableOIE, 2009
MaliNo information availableOIE, 2009
MauritiusNo information availableOIE, 2009
MoroccoNo information availableOIE, 2009
MozambiqueNo information availableOIE, 2009
NamibiaNo information availableOIE, 2009
NigeriaNo information availableOIE, 2009
SenegalNo information availableOIE, 2009
South AfricaNo information availableNULLHaenen et al., 2004; McVeigh, 2004; OIE, 2009
SudanDisease never reportedOIE, 2009
SwazilandNo information availableOIE, 2009
TanzaniaNo information availableOIE, 2009
TogoNo information availableOIE, 2009
TunisiaDisease not reportedOIE, 2009
UgandaNo information availableOIE, 2009
ZambiaNo information availableOIE, 2009
ZimbabweNo information availableOIE, 2009

North America

CanadaRestricted distributionOIE, 2009
GreenlandDisease never reportedOIE, 2009
MexicoDisease not reportedOIE, 2009
USAPresentNULLHedrick et al., 2000; OIE, 2009
-ArkansasPresentGoodwin, 2000
-CaliforniaPresentGray et al., 2002; Waltzek and Hedrick, 2004
-GeorgiaDisease never reportedOIE, 2009
-New YorkPresentHaenen et al., 2004
-South CarolinaPresentTerhune et al., 2004

Central America and Caribbean

BelizeDisease never reportedOIE, 2009
Costa RicaNo information availableOIE, 2009
CubaDisease never reportedOIE, 2009
El SalvadorNo information availableOIE, 2009
GuadeloupeNo information availableOIE, 2009
GuatemalaDisease never reportedOIE, 2009
HaitiNo information availableOIE, 2009
HondurasNo information availableOIE, 2009
JamaicaDisease never reportedOIE, 2009
MartiniqueNo information availableOIE, 2009
NicaraguaNo information availableOIE, 2009
PanamaNo information availableOIE, 2009

South America

ArgentinaDisease never reportedOIE, 2009
BoliviaNo information availableOIE, 2009
BrazilDisease never reportedOIE, 2009
ChileDisease never reportedOIE, 2009
ColombiaDisease never reportedOIE, 2009
EcuadorNo information availableOIE, 2009
French GuianaDisease not reportedOIE, 2009
PeruNo information availableOIE, 2009
UruguayNo information availableOIE, 2009
VenezuelaNo information availableOIE, 2009

Europe

AlbaniaNo information availableOIE, 2009
AustriaNo information availableNULLHaenen et al., 2004; OIE, 2009
BelarusNo information availableOIE, 2009
BelgiumNo information availableNULLHaenen et al., 2004; OIE, 2009
BulgariaNo information availableOIE, 2009
CroatiaDisease never reportedOIE, 2009
CyprusDisease never reportedOIE, 2009
Czech RepublicDisease not reportedOIE, 2009
DenmarkPresentNULLHaenen et al., 2004; OIE, 2009
EstoniaNo information availableOIE, 2009
FinlandDisease never reportedOIE, 2009
FranceNo information availableNULLHaenen et al., 2004; OIE, 2009
GermanyPresentNULLBretzinger et al., 1999; Haenen et al., 2004; Schlotfeldt, 2004; OIE, 2009
GreeceNo information availableOIE, 2009
HungaryDisease never reportedOIE, 2009
IcelandDisease never reportedOIE, 2009
IrelandDisease not reportedOIE, 2009
ItalyNo information availableNULLHaenen et al., 2004; OIE, 2009
LatviaDisease never reportedOIE, 2009
LiechtensteinNo information availableOIE, 2009
LithuaniaDisease never reportedOIE, 2009
LuxembourgNo information availableNULLHaenen et al., 2004; OIE, 2009
MacedoniaNo information availableOIE, 2009
MaltaNo information availableOIE, 2009
MontenegroNo information availableOIE, 2009
NetherlandsPresentNULLHaenen et al., 2004; OIE, 2009
NorwayDisease never reportedOIE, 2009
PolandNo information availableNULLHaenen et al., 2004; OIE, 2009
PortugalDisease never reportedOIE, 2009
RomaniaNo information availableOIE, 2009
Russian FederationNo information availableOIE, 2009
SerbiaNo information availableOIE, 2009
SlovakiaDisease not reportedOIE, 2009
SloveniaPresentOIE, 2009
SpainNo information availableOIE, 2009
SwedenDisease not reportedOIE, 2009
SwitzerlandDisease never reportedNULLHaenen et al., 2004; OIE, 2009
UKPresentNULLWalster, 1999; Denham, 2003; Haenen et al., 2004; OIE, 2009
UkraineDisease never reportedOIE, 2009

Oceania

AustraliaDisease never reportedOIE, 2009
French PolynesiaDisease never reportedOIE, 2009
New CaledoniaDisease never reportedOIE, 2009
New ZealandDisease never reportedOIE, 2009

Pathology

Top of page

Postmortem findings and histopathology.

The histological picture of diseased fish is one mainly of inflammation and necrosis, and the gill tissues usually show the most marked changes. It should be noted that all the following pathology does not occur in every diseased fish, and some pathology has not been observed at all in some of the outbreaks. For instance, intranuclear inclusions were reported in tissues from outbreaks in Israel and the USA (Hedrick et al., 2000), but were only rarely observed in the first Japanese outbreaks (Sano et al., 2004a,b), The reported histopathology for different organs and tissues is as follows:

Gills: Gill pathology was observed as early as 2 days post experimental infection (Pikarsky et al., 2003), and different aspects of the pathology have been described by Bretzinger et al. (1999), Walster (1999), Hedrick et al. (2000), Perelberg et al. (2003), Pikarsky et al. (2003), Sano et al. (2004a,b), Sunarto et al. (2004). A particular feature was hyperplasia and hypertrophy of branchial epithelium. Fusion of adjacent secondary lamellae was common and adhesion of gill filaments occurred. Small foci of necrotic cells were scattered among epithelial cells of the secondary lamellae, and focal sloughing of the surface epithelium of the gill progressed to the complete loss of lamellae. A mixed inflammatory cell infiltrate was seen in all gill filaments and eosinophilic granulocytes were seen in the epithelium of primary and secondary lamellae. There was congestion of the central sinus in the gill. Branchial epithelial cells and leucocytes in capillaries had prominent nuclear swelling, margination of chromatin and pale diffuse eosinophilic intranuclear inclusions were observed.

Kidney: After the gill, the kidney exhibits the most marked pathology (Walster, 1999; Pikarsky et al., 2003). There was a peritubular inflammatory cell infiltrate 2 days post infection followed by a heavy interstitial inflammatory cell infiltrate at 6 days post infection (Pikarsky et al., 2003). Nuclear inclusions were observed in haematopoietic cells (Hedrick et al., 2000), in glomeruli (Perelberg et al., 2003) and in some of the inflammatory interstitial cells. The wall of collecting duct of nephrons was frequently oedematous and cell infiltration was seen (Sano et al., 2004a,b). Necrosis of renal tubular epithelium and individual haematopoietic cells occurred (Hedrick et al., 2000; Pikarsky et al., 2003).

Spleen: The parenchyma had foci of necrosis, either as single cells or groups of cells. Some cells had intranuclear inclusions (Hedrick et al., 2000).

Liver: There were foci of necrosis, again either as single cells or groups of cells (Perelberg et al., 2003). Mild inflammatory infiltrates were seen in the parenchyma or in the walls of blood vessels (Bretzinger et al., 1999; Pikarsky et al., 2003; Sano et al., 2004a,b), and intranuclear inclusions were seen in lesions (Hedrick et al., 2000).

Pancreas: There was lymphocyte infiltration and sparse to severe necrosis of acinar cells (Bretzinger et al., 1999; Hedrick et al., 2000; Sano et al., 2004a,b).

Gut: Necrotic foci in gut mucosa were observed (Bretzinger et al., 1999).

Brain: Focal meningeal and parameningeal inflammation can occur (Walster, 1999; Pikarsky et al., 2003)

Oral epithelium: The oral epithelium was hyperplastic with foci of necrosis. A few cells had pale diffuse eosinophilic inclusions (Hedrick et al., 2000).

Skin: The epidermis separated from the basement membrane (Bretzinger et al., 1999).

The loss of osmoregulatory functions of the gill, gut and kidney are assumed to contribute to mortality (Gilad et al., 2004).

Pikarsky et al. (2003) used immunostaining methods to locate virus antigen. The fluorescent antibody test was applied to touch imprints of kidney, liver and brain of symptomatic experimentally-infected fish 16 days post infection. There were abundant virus antigen-positive cells in the kidney, and such cells were also observed in the liver and brain, but at a much lower frequency. Those authors also used immunohistochemistry to detect virus antigen in fish tissues. Virus proteins were detected in cells of the kidney interstitium 2 days post infection. The number of infected cells had increased by 6 days post infection, and stayed at the same level to 10 days post infection. At that time virus antigen was also seen in tubular epithelial cells. Virus antigen was observed in the liver at 2 days post infection. An increasing number of virus antigen-positive cells in gill tissue was observed between 2 and 10 days post infection. However, a small number of positive cells were observed in control gill tissues, which could represent the detection of sub-clinical carriers, detection of a serologically related virus or a cross-reaction with non-viral proteins present in the gills (Pikarsky et al., 2004). Ronen et al. (2003) detected a low level of antibody against KHV in the sera of naïve fish by the ELISA, and suggested that this might have been the result of cross-reaction with a non-viral contamination in the virus antigen used for the ELISA, or with cross-reacting virus (non-KHV) antigens.

KHV DNA was detected in experimentally infected fish using a real time PCR (Gilad et al., 2004). Viral DNA was detected in mucus, gill, liver, spleen, kidney, gut and brain 1 day post infection at 18, 23 and 28°C; the highest levels of DNA were in the brain and spleen at 28°C (3.25 × 1010 and 1.52 × 109 KHV genome equivalents per 106 cells, respectively). Likewise, KHV DNA was detected in blood and kidney 1 day post bath infection or 3-5 days post cohabitation infection by Pikarsky et al. (2004). KHV DNA can be detected by PCR in blood cells from naturally infected fish showing disease symptoms (Shapira eta al., 2005). Viral DNA was detected 62 days post infection in gill, kidney and brain of surviving fish (Gilad et al., 2004). Using dot blot DNA hybridization, Gray et al. (2002) detected viral DNA predominantly in gill and gut tissue, and to a lesser extent in liver and kidney of experimentally infected fish sampled 17-19 days post infection when clinical disease was occurring.

Diagnosis

Top of page

KHVD should be considered as a possible cause of disease of koi or common carp that are exhibiting the main clinical signs described under the Disease course section. Goodwin (2003) described how the clinical signs of KHVD may be distinguished from spring viraemia of carp and certain other diseases of carp. However, clinical signs alone are not sufficient for a definitive diagnosis of KHVD. That can only be done by isolation of the virus in cell culture and identification by a suitable method, such as PCR, or by identification of viral DNA directly in fish tissues. Shapira et al. (2005) suggested that the FAT on touch imprints of kidney could be used as a diagnostic method. However, the method needs careful validation as potential cross-reactions with other viral or non-viral antigens can occur (Pikarsky et al., 2004 and see Pathology section). Haenen et al. (2004) discussed the advantages and disadvantages of different methods for the diagnosis of KHV, and their conclusion was that the PCR was the most reliable method.

A number of different PCR methods, or variants of the method have been described (Gilad et al., 2002, 2003; Gray et al., 2002; Gunimaladevi et al., 2004; Pikarsky et al., 2004) that can detect KHV DNA in infected fish. The PCR detected more positive fish than virus isolation (Gilad et al., 2002; Haenen et al., 2004). The PCR described by Gilad et al. (2002) amplified DNA from KHV from Israel and the USA, but not from CHV-1 or CCV. Gilad et al. (2003) developed a real-time TaqMan PCR, and suggested that it was more sensitive that their initial PCR, but without providing a direct comparison. Their initial PCR could detect 1 pg of viral DNA, and the real time PCR could detect 10 copy numbers of target KHV sequence in a plasmid. The PCR of Gray et al. (2002) could detect 100 fg (approximately 600 DNA copies assuming a genome size of 140-180 kbp), increasing to 1 fg (6 DNA copies) following Southern blot hybridization using a digoxigenin-labelled probe. A loop-mediated isothermal (LAMP) method and a PCR for KHV DNA detection were developed by Gunimaladevi et al. (2004). Both methods had a similar sensitivity for detecting KHV DNA in gill tissue, but the LAMP method was more rapid. When both methods were compared using tissues from naturally infected fish, the LAMP method detected KHV DNA in gill, liver and kidney, whereas the PCR only detected the DNA in gills. Neither method detected viral DNA in spleen, gut, brain or heart.

Cell lines that are sensitive or refractory to KHV have been described in the Koi herpesvirus Pathogen Characteristics section. There is no consensus opinion, or data from comparative studies to show which tissue(s) should be taken for virus isolation. The following tissues have been taken for routine virus isolation on CCB or KF-1 cells: gill, kidney and spleen (Hedrick et al., 2000; Gilad et al., 2002, 2003), gill and kidney (Sano et al., 2004a), spleen and kidney (Terhune et al., 2004), gill, skin, liver, spleen and kidney (Neukirch and Kunz, 2001). Primary cultures of carp fin cells have been used for virus isolation by co-cultivation with kidney cells (Pikarsky et al., 2004) or liver and kidney cells (Hutoran et al., 2005) from diseased fish, but neither report provided details of how the liver or kidney cells for co-cultivation were obtained. Perelberg et al. (2003) inoculated the carp fin primary cells with a kidney extract.

It is essential that any virus isolated in cell culture should be identified by a PCR, LAMP or probe method before a diagnosis of KHVD can be made, as viruses other than KHV have been isolated during several separate investigations into carp mortalities, including cases where there were clinical signs of KHVD. Neukirch and Kunz (2001) investigated many cases of diseased koi carp with symptoms of KHVD in Germany. They isolated viruses that on the basis of morphology and nucleic acid type were likely to be paramyxovirus, orthomyxovirus, rhabdovirus, aquareovirus or aquabirnavirus in addition to herpesvirus. All the viruses were isolated in CCB and Ca F-2 cells, and all except the orthomyxovirus and herpesvirus were also isolated in EPC and CCG cells. A virus was isolated from liver, kidney and spleen extracts from a single koi carp from Germany exhibiting some of the signs of KHVD in CCG, CCB and EPC cells, but not in CHSE-214 or FHM cells (Neukirch et al., 1999). The virus was injected into koi carp, but no mortalities ensued, and the gill pathology observed may have been caused by an infection with Dactylogyrus sp. A paramyxo-like virus was isolated in EPC cells from gills, spleen and kidney of diseased koi carp imported into Belgium (Body et al., 2000). A similar virus has been isolated in EPC and KF-1 cells in the UK (Haenen et al., 2004). During investigations into a disease of koi carp in Korea causing gill pathology, a cytoplasmic virus 70-80 nm diameter was isolated from kidney and spleen tissues in FHM cells, but not in CHSE-214, RTG-2 or EPC cells (Oh et al., 2001). That virus was pathogenic for carp, producing similar clinical signs to the naturally diseased fish. Although the clinical signs were similar to KHVD, the description of the virus is different from KHV.

A number of laboratories are developing more sensitive PCR methods, or methods to screen for KHV antibodies in carp in order to detect carrier fish, or populations that have been exposed to the virus (Haenen et al., 2004).

List of Symptoms/Signs

Top of page
SignLife StagesType

Finfish

Adhesions - Body Cavity and Muscle Aquatic:Adult Sign
Adhesions - Body Cavity and Muscle Aquatic:Adult Sign
Bursts of abnormal activity - Behavioural Signs Aquatic:Adult Sign
Bursts of abnormal activity - Behavioural Signs Aquatic:Adult Sign
Cessation of feeding - Behavioural Signs Aquatic:Adult Sign
Cessation of feeding - Behavioural Signs Aquatic:Adult Sign
Dry skin (no mucus) - Skin and fins Aquatic:Adult Sign
Erosion - Gills Aquatic:Adult Diagnosis
Erosion - Gills Aquatic:Adult Diagnosis
Fouling - Gills Aquatic:Adult Sign
Fouling - Gills Aquatic:Adult Sign
Fusion of secondary lamellae - Gills Aquatic:Adult Diagnosis
Fusion of secondary lamellae - Gills Aquatic:Adult Diagnosis
Generalised lethargy - Behavioural Signs Aquatic:Adult Sign
Generalised lethargy - Behavioural Signs Aquatic:Adult Sign
Increased respiratory rate (increased opercular movements) - Behavioural signs Aquatic:Adult Sign
Increased respiratory rate (increased opercular movements) - Behavioural signs Aquatic:Adult Sign
Irregular colouration - Gills Aquatic:Adult Diagnosis
Irregular colouration - Gills Aquatic:Adult Diagnosis
Loss of balance - Behavioural Signs Aquatic:Adult Sign
Loss of balance - Behavioural Signs Aquatic:Adult Sign
Mortalities -Miscellaneous Aquatic:Adult Diagnosis
Mucus build up - Gills Aquatic:Adult Diagnosis
Mucus build up - Gills Aquatic:Adult Diagnosis
Pale, lightened or brightened colouration - Skin and fins Aquatic:Adult Sign
Pale, lightened or brightened colouration - Skin and fins Aquatic:Adult Sign
Red spots: pin-point size (petechiae) - Skin and Fins Aquatic:Adult Sign
Red spots: pin-point size (petechiae) - Skin and Fins Aquatic:Adult Sign
Scale loss - Skin and Fins Aquatic:Adult Sign
Skin erosion - Skin and Fins Aquatic:Adult Sign
Skin erosion - Skin and Fins Aquatic:Adult Sign
Sunken eyes - Eyes Aquatic:Adult Sign
Sunken eyes - Eyes Aquatic:Adult Sign
Torn, split, ragged or frayed fins - Skin and fins Aquatic:Adult Sign
Torn, split, ragged or frayed fins - Skin and fins Aquatic:Adult Sign

Disease Course

Top of page

Many of the recorded cases of the disease have occurred after the introduction of new fish into a culture system (e.g. garden ponds or dealers’ premises), or after mixing of fish at a koi show, and so the approximate time of contact between infected and naïve fish under non-laboratory conditions is known. The disease takes between 8-21 days to manifest itself under those conditions (Bretzinger et al., 1999, Walster, 1999, Hedrick et al., 2000) although it can take as little as 3 days for naïve fish added to a pond containing clinically diseased fish to show disease (Walster, 2003). Morbidity is usually 100%, and mortality is often 70-80% (Walster, 1999) but can be 100% (Bretzinger et al., 1999). In outbreaks of disease, mortality rates of 50% over a 10 day period (Hedrick et al., 2000) and 90% over a 14 day period (Tu et al., 2004a,b) have been reported. Under experimental conditions the virus can be transmitted by co-habitation, or by bath exposure of the fish to the virus, and the disease course is similar to the field experience. The virus can also be transmitted by iintraperitoneal injection. In cohabitation experiments, mortalities occurred 7-13 days post exposure (Bretzinger et al., 1999; Perelberg et al., 2003; Hutoren et al., 2005), and in a bath infection they occurred10-24 days post exposure (Pikarsky et al., 2004). Under experimental conditions the virus is infectious in the water for four hours, but not 21 hours (Perelberg et al., 2003). A contact time between virus (10-40 plaque-forming units [pfu]/ml water) and susceptible fish of a little as 5 minutes is sufficient to cause disease (Perelberg et al., 2005).

Diseased fish are usually lethargic, anorexic, often show rapid respiratory movements, and there are sometimes periods of hyperactivity and disorientation (Bretzinger et al.; 1999; Walster, 1999; Hedrick et al., 2000; Perelberg et al., 2003; Sano et al 2004a,b; Hutoran et al., 2005). The skin exhibits a focal or total loss of epidermis, pale discolouration, often a rough texture, under- or over-production of mucus and there may be reddening of the skin. There may be fin erosions, hemorrhages at fin bases, and the fish may have sunken eyes (enophthalmia) (Bretzinger et al., 1999; Walster, 1999; Hedrick et al., 2000; Denham, 2003; Perelberg et al., 2003; Sano et al 2004a,b). The gills usually show the most marked changes with an irregular colouration, necrosis and inflammation, swelling at the tips of the primary and secondary lamellae, erosion of primary lamellae, fusion of secondary lamellae and dark coloured mucus may trail from the gills (Bretzinger et al., 1999; Walster, 1999; Hedrick et al., 2000; Gray et al., 2002; Denham; 2003; Perelberg et al., 2003; Sano et al 2004; Sunarto et al., 2004; Terhune et al., 2004; Tu et al., 2004a,b; Hutoran et al., 2005). Internally there may be no obvious pathology, although the following have been observed: adhesions of internal organs (Hedrick et al., 2000), pale or dark organs (Bretzinger et al., 1999; Walster, 1999), enlarged liver (Perelberg et al., 2003) or kidney (Bretzinger et al., 1999), petechial haemorrhages on the liver and kidney (Walster, 1999).

The clinical signs of the disease in common carp in Korea caused by a herpes-like virus are very similar to those described for KHVD. The signs included dark skin, gill necrosis, haemorrhages at fin bases, enophthalmia and internally, adhesions of internal organs (Choi et al., 2004).

The body and gills of many fish suffering from KHVD are infested with ectoparasites, particularly protozoa (such as Ichthyobodo sp., Ichtyophthirius sp., Cryptobia sp., Chilodonella sp., Trichodina sp.), Dactylogyrus sp., Argulus sp., Gyrodactylus sp. and gill monogeneans (Bretzinger et al.,1999; Walster, 1999; Hedrick et al., 2000; Perelberg et al., 2003; Sano et al., 2004a,b). Numerous species of bacteria (Bretzinger et al., 1999; Walster, 1999; Hedrick et al., 2000; Terhune et al., 2004) have also been isolated from necrotic gill tissues. None of these organisms are thought to have a role in the disease, except for its possible transmission by Argulus sp. (Walster, 2000). Pikarsky et al. (2004) suggested that the microorganisms present on the gills were secondary and not the cause of the necrosis as they were first observed after the sloughing of gill epithelial cells started.

Antibodies against KHV produced in fish following experimental infection were detected by an enzyme-linked immunosorbent assay (ELISA) by Ronen et al. (2003). There was a high background absorbance in the assay, and the authors did not provide a criterion for a positive reading, but by day 21 post infection there was an increase of absorbance over background levels. Those levels were present at least until 51 days post infection.

Epidemiology

Top of page

The disease is easily spread horizontally by movement of infected fish, which has caused the rapid international dissemination of koi herpesvirus disease (KHVD). The disease was rapidly spread within Japan by the movement of infected fish, before it was known that they had KHV (Sano et al., 2004a,b). In the first year of outbreaks of KHVD in Indonesia infected fish were sold at a low price, which helped to spread the disease, and outbreaks in subsequent years can be traced to transfers of fish from infected areas (Sunarto et al., 2004) The introduction of KHVD into Indonesia was associated with the importation of fish from mainland China via Hong Kong. In the USA, the first outbreaks were in koi carp from a retail facility and in koi belonging to private owners 10-14 days after the fish had been exhibited at a koi show (Hedrick et al., 2000) where it is the usual practice to mix koi from different owners in the same tank. Such practices have been stopped at many subsequent koi shows as a measure to stop the spread of disease. KHVD occurred in lakes or ponds in public parks in Taiwan that had had no recent introductions of fish, and it was possible that the disease outbreaks in those systems were caused by the release of infected fish into the ponds by members of the public (Tu et al., 2004a). The disease has been passed between systems on infected sites by contaminated nets, hands and via aerosols, and there has been the suggestion that the carp louse (Argulus sp.) may play a part in the transmission of the disease (Walster, 1999, 2000). It is also possible that KHVD may be spread by predatory birds, such as herons, cormorants and ospreys (Schlotfeldt, 2004).

Impact Summary

Top of page
CategoryImpact
Environment (generally) Negative
Fisheries / aquaculture Negative
Other Negative
Trade/international relations Negative

Impact: Economic

Top of page

The disease has had a severe economic impact in many of the counties in which it occurs. It has affected the food carp production industry as well as the ornamental fish industry. Unlike some diseases that only affect certain life stages of fish, koi herpesvirus disease (KHVD) can affect all stages from fry to adult and can kill market-size food fish, and high value koi carp. There are both direct costs of loss of the fish, and also indirect costs of disinfection and fallowing sites, which often results in the loss of future production. It has caused loss of confidence in some parts of the ornamental fish industry and has also had an effect on koi carp as a hobby, and has caused the cancellation of numerous koi shows. In the three years since the first outbreak in Israel in 1998, KHVD spread to 90% of the carp farms (Perelberg et al., 2003). By the end of 1998 the losses of common carp and ornamental carp were estimated to be $1.2 million and $0.8 million annually. Since then the disease has cost $3 million annually. The loss of production of food carp in Israel in 1999 was estimated to be 1500 tons (Mires, 2001). In Japan, the disease first occurred in a lake used for common carp production, and in approximately one month over 1200 tonnes of fish had died, representing 25% of the annual production of the lake (Sano et al., 2004a) with a value of approximately $2.55 million (Waltzek et al., 2004). All remaining cultured carp in the lake were destroyed as a control measure (Sano et al., 2004b). The disease has only been detected in common carp and not in koi carp in Japan (Sano 2004b). In just two regions of Germany, the costs to three farms in 2003 were $435,500 and to one farm in 2004 was $417,000 (Schlotfeldt, 2004). Over 5000 koi farmers in East Java were affected by the first outbreak of KHVD in Indonesia (Sunarto et al., 2004) and the economic loss was estimated to be $0.5 million within the first three months of the outbreak. The socio-economic impact on affected communities was estimated to be $5 million in July of 2002, but by December of that year following the rapid spread of KHVD the figure had doubled; as of December 2003 the losses were estimated to be $15 million.

Zoonoses and Food Safety

Top of page

KHVD is not a zoonosis

References

Top of page

Body A; Lieffrig F; Charlier G; Collard A, 2000. Isolation of virus-like particles from koi (Cyprinus carpio) suffering gill necrosis. Bulletin of the European Association of Fish Pathologists, 20(2):87-88.

Bretzinger A; Fischer-Scherl T; Oumouna M; Hoffmann R; Truyen U, 1999. Mass mortalities in Koi carp, Cyprinus carpio, associated with gill and skin disease. Bulletin of the European Association of Fish Pathologists, 19(5):182-185.

Choi DL; Sohn SG; Bang JD; Do JW; Park MS, 2004. Ultrastructural identification of a herpes-like virus infection in common carp Cyprinus carpio in Korea. Diseases of Aquatic Organisms, 61:165-168.

Denham K, 2003. Koi herpesvirus in wild fish. Veterinary Record, 153(16):507.

Gilad O; Yun S; Adkison MA; Way K; Willits NH; Bercovier H; Hedrick RP, 2003. Molecular comparison of isolates of an emerging fish pathogen, koi herpesvirus, and the effect of water temperature on mortality of experimentally infected koi. Journal of General Virology, 84(10):2661-2668.

Gilad O; Yun S; Andree KB; Adkison MA; Amir Zlotkin; Bercovier H; Avi Eldar; Hedrick RP, 2002. Initial characteristics of koi herpesvirus and development of a polymerase chain reaction assay to detect the virus in koi, Cyprinus carpio koi. Diseases of Aquatic Organisms, 48(2):101-108.

Gilad O; Yun S; Zagmutt-Vergara FJ; Leutenegger CM; Bercovier H; Hedrick RP, 2004. Concentrations of a Koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Diseases of Aquatic Organisms, 60:179-187.

Goodwin A, 2000. A new koi virus. Aquaculture Magazine, 26 (2):25-26.

Goodwin AE, 2003. Differential diagnosis: SVCV vs KHV in koi. FHS/AFS Newsletter, 31:9-13.

Gray WL; Mullis L; LaPatra SE; Groff JM; Goodwin A, 2002. Detection of koi herpesvirus DNA in tissues of infected fish. Journal of Fish Diseases, 25(3):171-178.

Gunimaladevi I; Kono T; Venugopal MN; Sakai M, 2004. Detection of koi herpesvirus in common carp, Cyprinus carpio L., by loop-mediated isothermal amplification. Journal of Fish Diseases, 27:583-589.

Haenen OLM; Way K; Bergmann SM; Ariel E, 2004. The emergence of koi herpesvirus and its significance to European aquaculture. Bulletin of the European Association of Fish Pathologists, 24:293-307.

Hedrick RP; Gilad O; Yun S; Spangenberg JV; Marty GD; Nordhausen RW; Kebus MJ; Bercovier H; Eldar A, 2000. A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. Journal of Aquatic Animal Health, 12(1):44-57.

Huat LK; Kueh S; Kwang PY, 2004. Current status of transboundary fish diseases in Singapore: occurrence, surveillance, research and training. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department, 199-210.

Hutoran M; Ronen A; Perelberg A; Ilouze M; Dishon A; Bejerano I; Chen N; Kotler M, 2005. Description of an as yet unclassified DNA virus from diseased Cyprinus carpio species. Journal of Virology, 79:1983-1991.

Kanchanakhan S, 2004. Current status of transboundary fish diseases in Thailand: occurrence, surveillance, research and training. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department,.

McVeigh S, 2004. KHV identified in South Africa. Fish Farming International, 31:27.

Mires D, 2001. Forecasted supply and demand for comestible fish in Israel - 2001-2005. Israeli Journal of Aquaculture - Bamidgeh, 53(1):5-14.

Musa N; Leong LK; Sunarto A, 2005. Koi herpesvirus (KHV) - an emerging pathogen in koi. Colloquim on Viruses of Veterinary and Public Health Importance, Bangi, Malaysia, 146-147.

Neukirch M; Böttcher K; Bunnajirakul S, 1999. Isolation of a virus from koi with altered gills. Bulletin of the European Association of Fish Pathologists, 19(5):221-224.

Neukirch M; Kunz U, 2001. Isolation and preliminary characterization of several viruses from koi (Cyprinus carpio) suffering gill necrosis and mortality. Bulletin of the European Association of Fish Pathologists, 21(4):125-135.

Oh M-J; Jung S-J; Choi TJ; Kim H-R; Rajendran KV; Kim Y-J; Park M-A; Chun S-K, 2001. A viral disease occurring in cultured carp Cyprinus carpio in Korea. Fish Pathology, 36:147-151.

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

Perelberg A; Ronen A; Hutoran M; Smith Y; Kotler M, 2005. Protection of cultured Cyprinus carpio against a lethal viral disease by an attenuated virus vaccine. Vaccine, 23:3396-3403.

Perelberg A; Smirnov M; Hutoran M; Diamant A; Bejerano Y; Kotler M, 2003. Epidemiological description of a new viral disease afflicting cultured Cyprinus carpio in Israel. Israeli Journal of Aquaculture - Bamidgeh, 55(1):5-12.

Pikarsky E; Ronen A; Abramowitz J; Levavi-Sivan B; Hutoran M; Shapira Y; Steinitz M; Perelberg A; Soffer D; Kotler M, 2004. Pathogenesis of acute viral disease induced in fish by carp interstitial nephritis and gill necrosis virus. Journal of Virology, 78:9544-9551.

Regenmortel MHVvan; Fauquet CM; Bishop DHL; Carstens EB; Estes MK; Lemon SM; Maniloff J; Mayo MA; McGeoch DJ; Pringle CR; Wickner RB, 2000. Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. xii + 1162 pp.; many ref.

Regidor SE; Albaladejo; JD; Somga; JR, 2004. Current status of transboundary fish diseases in the Philippines: occurrence, surveillance, research and training. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department, 171-198.

Ronen A; Perelberg A; Abramowitz J; Hutoran M; Tinman S; Bejerano I; Steinitz M; Kotler M, 2003. Efficient vaccine against the virus causing a lethal disease in cultured Cyprinus carpio. Vaccine, 21(32):4677-4684.

Sano M; Ito T; Kurita J; Yanai T; Watanabe N; Miwa S; Iida T, 2004. First detection of koi herpesvirus in cultured common carp Cyprinus carpio in Japan. Fish Pathology, 39:165-167.

Sano M; Ito T; Kurita J; Yuasa K; Miwa S; Iida T, 2004. Experience on common carp mass mortality in Japan. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department, 13-19.

Schlotfeldt HF, 2004. Severe losses of common carp in Germany due to Koi Herpesvirus (KHV). Bulletin of the European Association of Fish Pathologists, 24:216-217.

Shapira Y; Magen Y; Zak T; Kotler M; Hulata G; evavi-Sivan B, 2005. Differential resistance to koi herpes virus (KHV)/carp interstitial nephritis and gill necrosis virus (CNGV) among common carp (Cyprinus carpio L.) strains and crossbreds. Aquaculture, 245:1-11.

Sunarto A; Widodo T; Koesharyani I; Supriyadi H; Gardenia L; Sugianti B; Rukmono D, 2004. Transboundary fish diseases in Indonesia: occurrence, surveillance, research and training. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department, 91-121.

Terhune JS; Grizzle JM; Hayden K; McClenahan SD, 2004. First report of koi herpesvirus in wild common carp in the Western Hemisphere. FHS/AFS Newslett, 32:8-9.

Theungphachanh T, 2004. Current status of transboundary fish diseases in Lao PDR: occurrence, surveillance, research and training. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department, 123-130.

Tu C; Lin SY; Sung HT, 2004. Current status of koi herpesvirus disease in Taiwan. In: Lavilla-Pitogo CR, Nagasawa K, eds. Transboundary Fish Diseases in Southeast Asia: Occurrence, Surveillance, Research and Training. Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department, 21-24.

Tu C; Weng MC; Shiau JR; Lin SY, 2004. Detection of koi herpesvirus in koi Cyprinus carpio in Taiwan. Fish Pathology, 39:109-110.

Walster C, 2003. A note on Koi Herpes Virus (KHV): current situation and issues arising. Fish Veterinary Journal, No.7:77-81.

Walster CI, 1999. Clinical observations of severe mortalities in koi carp, Cyprinus carpio, with gill disease. Fish Veterinary Journal, No. 3:54-58.

Walster CI, 2000. Koi carp mortality syndrome: an update. Fish Veterinary Journal, No. 5:72-75.

Waltzek TB; Hedrick RP, 2004. Koi herpesvirus update 2004. California Veterinarian, July-August: 14-16.

Distribution Maps

Top of page
You can pan and zoom the map
Save map
Download KML file Download CSV file
Creative Commons Licence
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.

Please click OK to ACCEPT or Cancel to REJECT

Creative Commons Licence
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.

Please click OK to ACCEPT or Cancel to REJECT