koi herpesvirus; Cyprinid herpesvirus 3; portal of entry; Cyprinus carpio
Abstract :
[en] Cyprinid herpesvirus 3 (CyHV-3), also known as Koi herpesvirus, is the etiological agent of a mortal disease in common and koi carp. Recently, we investigated the entry of CyHV-3 in carp using bioluminescence imaging and a CyHV-3 recombinant strain expressing luciferase (LUC). We demonstrated that the skin is the major portal of entry after inoculation of carp by immersion in water containing CyHV-3. While this model of infection mimics some natural conditions in which infection takes place, other epidemiological conditions could favour entry of virus through the digestive tract. Here, we investigated whether ingestion of infectious materials mediates CyHV-3 entry through the digestive tract. Carp were fed with materials contaminated with the CyHV-3 LUC recombinant (oral contamination) or immersed in water containing the virus (contamination by immersion). Bioluminescence imaging analyses performed at different times post-infection led to the following observations: (i) the pharyngeal periodontal mucosa is the major portal of entry after oral contamination, while the skin is the major portal of entry after contamination by immersion. (ii) Both modes of inoculation led to the spreading of the infection to the various organs tested. However, the timing and the sequence in which some of the organs turned positive were different between the two modes of inoculation. Finally, we compared the disease induced by the two inoculation modes. They led to comparable clinical signs and mortality rate. The results of the present study suggest that, based on epidemiological conditions, CyHV-3 can enter carp either by skin or periodontal pharyngeal mucosal infection.
Research Center/Unit :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Fournier, Guillaume ; Université de Liège - ULiège > Immunologie et vaccinologie
Boutier, Maxime ; Université de Liège - ULiège > Immunologie et vaccinologie
Victor, Stalin Raj
Mast, Jan
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Vanderwalle, Pierre
Peeters, Dominique ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Médecine interne des animaux de compagnie
Lieffrig, François
Farnir, Frédéric ; Université de Liège - ULiège > Département de productions animales > Biostatistiques et bioinformatique appliquées aux sc. vétér.
Gillet, Laurent ; Université de Liège - ULiège > Immunologie et vaccinologie
Feeding Cyprinus carpio with infectious materials mediates cyprinid herpesvirus 3 entry through infection of pharyngeal periodontal mucosa
Publication date :
25 January 2012
Journal title :
Veterinary Research
ISSN :
0928-4249
eISSN :
1297-9716
Publisher :
EDP Sciences, Les Ulis, France
Volume :
43
Issue :
6
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE] ULiège - Université de Liège [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Mass mortalities in koi, Cyprinus carpio, associated with gill and skin disease. Bretzinger A, Fischer-Scherl T, Oumouma R, Hoffmann R, Truyen U, Bull Eur Assoc Fish Pathol 1999 19 182 185 (Pubitemid 129622971)
An herpesvirus associated with mass mortality of juvenile and adult koi Cyprinus carpio. Hedrick RP, Marty R, Nordhausen M, Kebus M, Bercovier H, Eldar A, Fish Health Newsletter, FHS, Am Fish Soc 1999 27 7
A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. Hedrick RP, Gilad O, Yun S, Spangenberg J, Marty R, Nordhausen M, Kebus M, Bercovier H, Eldar A, J Aquat Anim Health 2000 12 44 55 10.1577/1548-8667(2000)012<0044:AHAWMM>2.0.CO;2
Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research. Michel B, Fournier G, Lieffrig F, Costes B, Vanderplasschen A, Emerg Infect Dis 2010 16 1835 1843 21122210
Clinical observations of severe mortalities in koi carp, Cyprinus carpio, with gill disease. Walster C, Fish Vet J 1999 3 54 58
Global distribution of KHV with particular reference to Europe. Haenen OL, Engelsma M, International Workshop on Koi Herpesvirus; London; 2004
Movement of pathogens with the international trade of live fish: problems and solutions. Hedrick RP, Rev Sci Tech 1996 15 523 531 8890378 (Pubitemid 126329023)
Genome sequences of three koi herpesvirus isolates representing the expanding distribution of an emerging disease threatening koi and common carp worldwide. Aoki T, Hirono I, Kurokawa K, Fukuda H, Nahary R, Eldar A, Davison AJ, Waltzek TB, Bercovier H, Hedrick RP, J Virol 2007 81 5058 5065 10.1128/JVI.00146-07 17329333 (Pubitemid 46744417)
Cloning of the koi herpesvirus genome as an infectious bacterial artificial chromosome demonstrates that disruption of the thymidine kinase locus induces partial attenuation in Cyprinus carpio koi. Costes B, Fournier G, Michel B, Delforge C, Raj VS, Dewals B, Gillet L, Drion P, Body A, Schynts F, Lieffrig F, Vanderplasschen A, J Virol 2008 82 4955 4964 10.1128/JVI.00211-08 18337580 (Pubitemid 351657057)
The major portal of entry of koi herpesvirus in cyprinus carpio is the skin. Costes B, Stalin Raj V, Michel B, Fournier G, Thirion M, Gillet L, Mast J, Lieffrig F, Bremont M, Vanderplasschen A, J Virol 2009 83 2819 2830 10.1128/JVI.02305-08 19153228
Bioluminescence imaging of live infected salmonids reveals that the fin bases are the major portal of entry for Novirhabdovirus. Harmache A, LeBerre M, Droineau S, Giovannini M, Bremont M, J Virol 2006 80 3655 3659 10.1128/JVI.80.7.3655-3659.2006 16537634
Detection of carp interstitial nephritis and gill necrosis virus in fish droppings. Dishon A, Perelberg A, Bishara-Shieban J, Ilouze M, Davidovich M, Werker S, Kotler M, Appl Environ Microbiol 2005 71 7285 7291 10.1128/AEM.71.11.7285-7291.2005 16269770 (Pubitemid 43194223)
Concentrations of a Koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Gilad O, Yun S, Zagmutt-Vergara FJ, Leutenegger CM, Bercovier H, Hedrick RP, Dis Aquat Organ 2004 60 179 187 15521316 (Pubitemid 39588252)
Detection of KHV in freshwater mussels and crustaceans from ponds with khv history in common carp (Cyprinus carpio). Kielpinski M, Kempter J, Panicz R, Sadowski J, Schütze H, Ohlemeyer S, Bergmann SM, Isr J Aquaculture 2010 62 28 37
Chemical senses, chemical signals and feeding behavior in fishes. Atema J, Fish Behavior and its use in the capture and culture of fishes Manila: ICLARM, Bardach JE, Magnuson JJ, May RC, Reinhart JM, 1980 5 512
Gustatory control of feeding behavior in goldfish. Lamb CF, Finger TE, Physiol Behav 1995 57 483 488 10.1016/0031-9384(94)00287-F 7753885
Specializations and limitations in the utilization of food resources by the carp, Cyprinus carpio: a study of oral food processing. Sibbing F, Environ Biol Fishes 1988 22 161 178 10.1007/BF00005379 (Pubitemid 19321742)
Internal anatomy of common carp (Cyprinus carpio) as revealed by magnetic resonance imaging. Kalat T, Shabanipour N, Appl Magn Reson 2010 38 361 369 10.1007/s00723-010-0122-3
Ultrastructural changes of the tracheal epithelium after vaccination of day-old chickens with the La Sota strain of Newcastle disease virus. Mast J, Nanbru C, van den Berg T, Meulemans G, Vet Pathol 2005 42 559 565 10.1354/vp.42-5-559 16145202 (Pubitemid 41279670)
Skin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells. Raj VS, Fournier G, Rakus K, Ronsmans M, Ouyang P, Michel B, Delforges C, Costes B, Farnir F, Leroy B, Wattiez R, Melard C, Mast J, Lieffrig F, Vanderplasschen A, Vet Res 2011 42 92 10.1186/1297-9716-42-92 21816061
Investigation of koi herpesvirus latency in koi. Eide KE, Miller-Morgan T, Heidel JR, Kent ML, Bildfell RJ, Lapatra S, Watson G, Jin L, J Virol 2011 85 4954 4962 10.1128/JVI.01384-10 21389134
Histopathological and ultrastructural features of Koi herpesvirus (KHV)-infected carp Cyprinus carpio, and the morphology and morphogenesis of KHV. Miyazaki T, Kuzuya Y, Yasumoto S, Yasuda M, Kobayashi T, Dis Aquat Organ 2008 80 1 11 18714678 (Pubitemid 352001027)
Epidemiological description of a new viral disease afflicting cultured Cyprinus Carpio in Israel. Perelberg A, Smirnov M, Hutoran M, Diamant A, Bejerano Y, Kotler M, Isr J Aquaculture 2003 55 5 12 (Pubitemid 37178233)
Pathogenesis of acute viral disease induced in fish by carp interstitial nephritis and gill necrosis virus. Pikarsky E, Ronen A, Abramowitz J, Levavi-Sivan B, Hutoran M, Shapira Y, Steinitz M, Perelberg A, Soffer D, Kotler M, J Virol 2004 78 9544 9551 10.1128/JVI.78.17.9544-9551.2004 15308746 (Pubitemid 39096561)