Susceptibility of the topmouth gudgeon (Pseudorasbora parva) to CyHV-3 under no-stress and stress conditions

https://doi.org/10.17221/88/2017-VETMEDCitation:Pospichal A, Pokorova D, Vesely T, Piackova V (2018): Susceptibility of the topmouth gudgeon (Pseudorasbora parva) to CyHV-3 under no-stress and stress conditions. Veterinarni Medicina, 63: 229-239.
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Cyprinid herpesvirus 3 (CyHV-3), also known as koi herpesvirus, is the causative agent of the highly contagious koi herpesvirus disease, which is restricted to koi and common carp and causes significant losses in both fish stock. Some experimental investigations have shown that other cyprinid or non-cyprinid species may be asymptomatically susceptible to this virus and might play roles as potential carriers of CyHV-3 or might contribute to persistence of this virus in environment. Therefore, it seems important to verify not only the susceptibility of other cyprinid or non-cyprinid species, but also their ability to transmit CyHV-3 infection to susceptible species. Our previous investigation of the susceptibility of the topmouth gudgeon (Pseudorasbora parva) did not reveal the presence of CyHV-3 DNA in the tissues of this species after cohabitation with infected koi. Consequently, we changed the experimental conditions and applied two stress factors (removal of skin mucus and scaring) which would presumably mimic the stress most commonly encountered in the wild. Both experiments (without and with stress factors) consisted of primary and secondary challenges. In both the no-stress and stress experiments, the first challenge was focused only on testing the susceptibility of the topmouth gudgeon to the virus. With the secondary challenge, we investigated potential viral transmission from the topmouth gudgeon to healthy naive koi after exposure to stress factors. All fish (dead, surviving and sacrificed) were tested for the presence of CyHV-3 DNA using nested PCR (no-stress experiment) and real-time PCR (stress experiment). After the primary challenge of the no-stress experiment, PCR did not reveal the presence of CyHV-3 DNA in any specimen of cohabitated topmouth gudgeon, but all specimens of dead koi were CyHV-3 DNA-positive. PCR of fish tissues subjected to the secondary challenge did not show the transfer of virus to naive fish. After exposure to stress (removal of skin mucus), qPCR revealed four out of five samples (80%) of topmouth gudgeon to be positive for CyHV-3 DNA. Two out of five samples (40%) of topmouth gudgeon treated by scaring were found to be positive for the presence of viral DNA. Real-time PCR after the secondary challenge did not reveal any viral DNA positivity in specimens of topmouth gudgeon from groups previously exposed to stress. The stress experiments show that removal of skin mucus might potentially lead to susceptibility of topmouth gudgeon to CyHV-3 infection, but the transmission of the virus to koi carp was not observed.

References:
Adamek Mikołaj, Syakuri Hamdan, Harris Sarah, Rakus Krzysztof Ł., Brogden Graham, Matras Marek, Irnazarow Ilgiz, Steinhagen Dieter (2013): Cyprinid herpesvirus 3 infection disrupts the skin barrier of common carp (Cyprinus carpio L.). Veterinary Microbiology, 162, 456-470 https://doi.org/10.1016/j.vetmic.2012.10.033
 
Adamek Mikołaj, Steinhagen Dieter, Irnazarow Ilgiz, Hikima Jun-ichi, Jung Tae-Sung, Aoki Takashi (2014): Biology and host response to Cyprinid herpesvirus 3 infection in common carp. Developmental & Comparative Immunology, 43, 151-159 https://doi.org/10.1016/j.dci.2013.08.015
 
Antychowicz J, Reichert M, Matras M, Bergmann SM, Haenen O (2005): Epidemiology, pathogenicity and molecular biology of koi herpesvirus isolated in Poland. Bulletin of the Veterinary Institute in Pulawy 49, 367–373.
 
Bansil Rama, Turner Bradley S. (2006): Mucin structure, aggregation, physiological functions and biomedical applications. Current Opinion in Colloid & Interface Science, 11, 164-170 https://doi.org/10.1016/j.cocis.2005.11.001
 
Bercovier H, Fishman Y, Nahary R, Sinai S, Zlotkin A, Eyngor M, Gilad O, Eldar A, Hedrick RP (2005): Cloning of the koi herpesvirus (KHV) gene encoding thymidine kinase and its use for a highly sensitive PCR based diagnosis. BMC Microbiology 5, 13.https://doi.org/10.1186/1471-2180-5-13
 
Bergmann SM, Schutze H, Fisher U, Fichtner D, Riechardt M, Meyer K, Schrudde D, Kempter J (2009): Detection KHV genome in apparently healthy fish. Bulletin of European Association of Fish Pathologists 29, 145–152.
 
Bergmann SM, Lutze P, Schutze H, Fischer U, Dauber M, Fichtner D, Kempter J (2010): Goldfish (Carassius auratus auratus) is a susceptible species for koi herpesvirus (KHV) but not for KHV disease (KHVD). Bulletin of European Association of Fish Pathologists 30, 74–78.
 
Bretzinger A, Fuscher-Scherl T, Oumouna M, Hoffmann R, Truyen U (1999): Mass mortalities in koi carp, Cyprinus carpio, associated with gill and skin disease. Bulletin of European Association of Fish Pathologists 19, 182–185.
 
Dishon A., Perelberg A., Bishara-Shieban J., Ilouze M., Davidovich M., Werker S., Kotler M. (2005): Detection of Carp Interstitial Nephritis and Gill Necrosis Virus in Fish Droppings. Applied and Environmental Microbiology, 71, 7285-7291 https://doi.org/10.1128/AEM.71.11.7285-7291.2005
 
Eide Kathleen, Miller-Morgan Tim, Heidel Jerry, Bildfell Rob, Jin Ling (2011): Results of total DNA measurement in koi tissue by Koi Herpes Virus real-time PCR. Journal of Virological Methods, 172, 81-84 https://doi.org/10.1016/j.jviromet.2010.12.012
 
Ellis A.E (2001): Innate host defense mechanisms of fish against viruses and bacteria. Developmental & Comparative Immunology, 25, 827-839 https://doi.org/10.1016/S0145-305X(01)00038-6
 
El-Matbouli Mansour, Soliman Hatem (2011): Transmission of Cyprinid herpesvirus-3 (CyHV-3) from goldfish to naïve common carp by cohabitation. Research in Veterinary Science, 90, 536-539 https://doi.org/10.1016/j.rvsc.2010.07.008
 
EURL – European Union Reference Laboratory for Fish Diseases (2015): Diagnostic methods and procedures for the surveillance and confirmation of KHV disease. Official Journal of the European Union L 247, 45–48. Available at www.eurl-fish.eu/diagnostic_manuals/khv.
 
Fabian M, Baumer A, Steinhagen D (2012): Do wild fish species contribute to the transmission of koi herpesvirus to carp in hatchery ponds? Journal of Fish Diseases 36, 505–514.
 
Flamm A, Fabian M, Runge M, Böttcher K, Bräuer G, Füllner G, Steinhagen D (2016): Draining and liming of ponds as an effective measure for containment of CyHV-3 in carp farms. Diseases of Aquatic Organisms, 120, 255-260 https://doi.org/10.3354/dao03024
 
Fontenot DK, Neiffer DL (2004): Wound management in teleost fish: biology of the healing process, evaluation, and treatment. Veterinary Clinics of North America: Exotic Animal Practice 7, 57–86.
 
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 https://doi.org/10.3354/dao060179
 
Hedrick R. P., Gilad O., Yun S., Spangenberg J. V., Marty G. D., Nordhausen R. W., Kebus M. J., 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, 44-57 https://doi.org/10.1577/1548-8667(2000)012<0044:AHAWMM>2.0.CO;2
 
Hedrick RP, Gilad O, Yun SC, McDowell TS, Waltzek TB, Kelly GO, Adkison MA (2005): Initial isolation and characterization of a herpes-like virus (KHV) from Koi and ommon carp. Bulletin of Fisheries Research Agency 2, V7.
 
Hellio Claire, Pons Anne Marie, Beaupoil Claude, Bourgougnon Nathalie, Gal Yves Le (2002): Antibacterial, antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus. International Journal of Antimicrobial Agents, 20, 214-219 https://doi.org/10.1016/S0924-8579(02)00172-3
 
Kempter J, Sadowski J, Schutze H, Fischer U, Dauber M, Fichtner D, Panicz R, Bergmann SM (2009): Koi herpesvirus: Do acipenserid restitution programs pose a threat to carp farms in the disease-free zones? Acta Ichtyologica et Piscatoria 39, 119–126.
 
Kempter J, Kielpinski M, Panicz R, Sadowski J, Myslowski B, Bergmann SM (2012): Horizontal transmission of koi herpesvirus (KHV) from potential vector species to common carp. Bulletin of European Association of Fish Pathologists 32, 212–219.
 
Lemaître Christelle, Orange Nicole, Saglio Philippe, Saint Nathalie, Gagnon Jean, Molle Gérard (1996): Characterization and Ion Channel Activities of Novel Antibacterial Proteins from the Skin Mucosa of Carp ( Cyprinus carpio ). European Journal of Biochemistry, 240, 143-149 https://doi.org/10.1111/j.1432-1033.1996.0143h.x
 
Margaritov NM, Kiritsis SG (2011): Parasites of Topmouth gudgeon Psudorasbora parva (Schlegel) in fish farms in Bulgaria. Acta Zoologica Bulgarica 63, 187–193.
 
Matras Marek, Antychowicz Jerzy, Castric Jeannette, Bergmann Sven M. (2012): CYHV-3 Infection Dynamics in Common Carp (Cyprinus Carpio) – Evaluation of Diagnostic Methods. Bulletin of the Veterinary Institute in Pulawy, 56, - https://doi.org/10.2478/v10213-012-0023-3
 
McColl KA (2013): Review of the Literature on Cyprinid Herpesvirus 3 (CyHV-3) and its Disease. PestSmart Toolkit Publication, Canberra. 35 pp.
 
McGuckin Michael A., Lindén Sara K., Sutton Philip, Florin Timothy H. (2011): Mucin dynamics and enteric pathogens. Nature Reviews Microbiology, 9, 265-278 https://doi.org/10.1038/nrmicro2538
 
Miyazaki T, Kuzuya Y, Yasumoto S, Yasuda M, Kobayashi T (2008): Histopathological and ultrastructural features of Koi herpesvirus (KHV)-infected carp Cyprinus carpio, and the morphology and morphogenesis of KHV. Diseases of Aquatic Organisms, 80, 1-11 https://doi.org/10.3354/dao01929
 
Mohi El-Din MM (2011): Histopathological studies in experimentally infected koi carp (Cyprinus carpio koi) with koi herpesvirus in Japan. World Journal of Fish and Marine Sciences 3, 252–259.
 
Monaghan S J, Thompson K D, Adams A, Bergmann S M (2015): Sensitivity of seven PCRs for early detection of koi herpesvirus in experimentally infected carp, Cyprinus carpio L., by lethal and non-lethal sampling methods. Journal of Fish Diseases, 38, 303-319 https://doi.org/10.1111/jfd.12235
 
Negenborn J (2009): Klinisch-843 chemische parameter im blut und urin von karpfen unter infection mit dem koi-herpesvirus. [PhD Thesis.] University of Veterinary Medicine in Hannover, Hannover, Germany. 116 pp.
 
Neukirch M, Bottcher K, Sumrarn B (1999): Isolation of a virus from koi with altered gills. Bulletin of the European Association of Fish Pathologists 19, 221–224.
 
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 https://doi.org/10.1128/JVI.78.17.9544-9551.2004
 
Pokorova D., Reschova S., Hulova J., Vicenova M., Vesely T., Piackova V. (2010): Detection of Cyprinid Herpesvirus-3 in Field Samples of Common and Koi Carp by Various Single-Round and Nested PCR Methods. Journal of the World Aquaculture Society, 41, 773-779 https://doi.org/10.1111/j.1749-7345.2010.00419.x
 
Radosavljevic Vladimir, Jeremic Svetlana, Cirkovic M., Lako B., Milicevic Vesna, Potkonjak A., Nikolin V. (2012): Common fish species in polyculture with carp as cyprinid herpes virus 3 carriers. , 62, 675-681 https://doi.org/10.2298/AVB1206675R
 
Raj Victor, Fournier Guillaume, Rakus Krzysztof, Ronsmans Maygane, Ouyang Ping, Michel Benjamin, Delforges Cédric, Costes Bérénice, Farnir Frédéric, Leroy Baptiste, Wattiez Ruddy, Melard Charles, Mast Jan, Lieffrig François, Vanderplasschen Alain (2011): Skin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells. Veterinary Research, 42, 92- https://doi.org/10.1186/1297-9716-42-92
 
Rakus Krzysztof, Ouyang Ping, Boutier Maxime, Ronsmans Maygane, Reschner Anca, Vancsok Catherine, Jazowiecka-Rakus Joanna, Vanderplasschen Alain (2013): Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research. Veterinary Research, 44, 85- https://doi.org/10.1186/1297-9716-44-85
 
Reed A. N., Izume S., Dolan B. P., LaPatra S., Kent M., Dong J., Jin L. (2014): Identification of B Cells as a Major Site for Cyprinid Herpesvirus 3 Latency. Journal of Virology, 88, 9297-9309 https://doi.org/10.1128/JVI.00990-14
 
Ringø Einar, Myklebust Reidar, Mayhew Terry M., Olsen Rolf Erik (2007): Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture, 268, 251-264 https://doi.org/10.1016/j.aquaculture.2007.04.047
 
Roberts Rj, Ellis AE (2012): 2 The anatomy and physiology of teleosts. In: Roberts RJ (ed.): Fish Pathology. 4th edn. Willey-Blackwell. 17–61.
 
Rosecchi Elisabeth, Thomas Frederic, Crivelli Alain J. (2001): Can life-history traits predict the fate of introduced species? A case study on two cyprinid fish in southern France. Freshwater Biology, 46, 845-853 https://doi.org/10.1046/j.1365-2427.2001.00715.x
 
Schauber Jürgen, Gallo Richard L. (2008): Antimicrobial peptides and the skin immune defense system. Journal of Allergy and Clinical Immunology, 122, 261-266 https://doi.org/10.1016/j.jaci.2008.03.027
 
Simon Andrea, Britton Robert, Gozlan Rodolphe, van Oosterhout Cock, Volckaert Filip A. M., Hänfling Bernd, Steinke Dirk (2011): Invasive Cyprinid Fish in Europe Originate from the Single Introduction of an Admixed Source Population Followed by a Complex Pattern of Spread. PLoS ONE, 6, e18560- https://doi.org/10.1371/journal.pone.0018560
 
Thornton D. J. (2004): From Mucins to Mucus: Toward a More Coherent Understanding of This Essential Barrier. Proceedings of the American Thoracic Society, 1, 54-61 https://doi.org/10.1513/pats.2306016
 
van der Marel Maria, Adamek Mikołaj, Gonzalez Santiago F., Frost Patrick, Rombout Jan H.W.M., Wiegertjes Geert F., Savelkoul Huub F.J., Steinhagen Dieter (2012): Molecular cloning and expression of two β-defensin and two mucin genes in common carp (Cyprinus carpio L.) and their up-regulation after β-glucan feeding. Fish & Shellfish Immunology, 32, 494-501 https://doi.org/10.1016/j.fsi.2011.12.008
 
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