Investigation of the presence of nervous necrosis virus (NNV) in pikeperch (Sander lucioperca) and crayfish (Pontastacus leptodactylus)

Hakan Eren; Sibel Yavru

doi:10.12714/egejfas.43.1.01

TR EN

Sudak (Sander lucioperca) ve kerevitte (Pontastacus leptodactylus) nervöz nekrozis virüsünün (NNV) varlığının araştırılması

Öz

Bu çalışmada, göçmen kuşlar için önemli durak noktaları olan Eğirdir, Beyşehir ve Suğla göllerinde yaşayan sudak (Sander lucioperca) ve kerevitlerden (Pontastacus leptodactylus) NNV varlığı araştırılmıştır. 2022 yılında Eğirdir, Beyşehir ve Suğla göllerinden 3 farklı su sıcaklığı döneminde (15-20°C, 20-25°C ve 25-30°C) kerevit ve sudak örnekleri alınmıştır. Toplam 540 örnek (270 sudak ve kerevit) gerçek zamanlı RT-PCR ile NNV genomunun (RNA-1 ve RNA2) varlığı açısından analiz edilmiş ve ayrıca E-11 hücresine inokule edilmiştir. Hiçbir teknikle pozitif örnek kaydedilmemiştir. Bu çalışmada, Türkiye'nin tatlı sularında yaşayan yabani sucul organizmalarda NNV'nin varlığı ilk kez araştırılmış ve örneklenen sudak ve kerevitlerde NNV tespit edilmemiştir. Çalışmanın yapıldığı tarihte virusa rastlanılmamış olsada, göçmen kuşların göç yolları üzerinde bulunan bu göllerin NNV açısından düzenli olarak incelenmesinin önemli olduğu düşünülmektedir.

Anahtar Kelimeler

Destekleyen Kurum

This research was supported and funded by the General Directorate of Agricultural Research and Policies (TAGEM), Ministry of Agriculture and Forestry of the Republic of Türkiye, under Project No: TAGEM/HSGYAD/B/22/A5/P4/5421. The study is also derived from the doctoral dissertation submitted by Hakan Eren to the Institute of Health Sciences, Selçuk University.

Proje Numarası

Project No: TAGEM/HSGYAD/B/22/A5/P4/5421.

Etik Beyan

This study was conducted in accordance with the principles outlined in the Directive of the Animal Experiments Local Ethics Committee of the Eğirdir Fisheries Research Institute Directorate, affiliated with the General Directorate of Agricultural Research and Policies (TAGEM), Ministry of Agriculture and Forestry of the Republic of Türkiye. Ethical approval was granted by the committee on 28 April 2021 (Decision No: 01).

Teşekkür

I would like to thank Dr. Gülnur Kalaycı, Dr. Tuncay Vural, Dr. Murat Kaplan, Dr. Vedat Yegen, Dr. Kemal Pekmez, Dr. Oğuz Yaşar Uzunmehmetoğlu, İsmail Hakkı Öztuna, and Rahmi Uysal for their valuable help and support during this study. I am also especially grateful to Dr. Isabel Bandín for her scientific advice and guidance.

Kaynakça

Agrebi, H., Abbadi, M., Buratin, A., Biasini, L., Sghaier, H., Bouhaouala-Zahar, B., Toffan, A., & Cherif, N. (2025). Near-complete genome sequence of a reassortant fish nervous necrosis virus isolated from a European sea bass (Dicentrarchus labrax) in Tunisia. Microbiology resource announcements, 14(10), e0005825. https://doi.org/10.1128/mra.00058-25
Athanassopoulou, F., Billinis, C., & Prapas, T. (2004). Important disease conditions of newly cultured species in intensive freshwater farms in Greece: First incidence of nodavirus infection in Acipenser sp. Diseases of Aquatic Organisms, 60(3), 247 252. https://doi.org/10.3354/dao060247
Bandín, I., & Souto, S. (2020). Betanodavirus and VER disease: A 30-year research review. Pathogens, 9(2), 106. https://doi.org/10.3390/pathogens9020106
Bigarré, L., Cabon, J., Baud, M., Heimann, M., Body, A., Lieffrig, F., & Castric, J. (2009). Outbreak of betanodavirus infection in tilapia, Oreochromis niloticus (L.), in fresh water. Journal of Fish Diseases, 32(8), 667–673. https://doi.org/10.1111/j.1365-2761.2009.01037.x
Binesh, C.P. (2013). Mortality due to viral nervous necrosis in zebrafish Danio rerio and goldfish Carassius auratus. Diseases of Aquatic Organisms, 104(3), 257–260. https://doi.org/10.3354/dao02605
Bitchava, K., Chassalevris, T., Lampou, E., Athanassopoulou, F., Economou, V., & Dovas, C.I. (2019). Occurrence and molecular characterization of betanodaviruses in fish and invertebrates of the Greek territorial waters. Journal of Fish Diseases, 42(12), 1773 1783. https://doi.org/10.1111/jfd.13098
Boukedjouta, R., Pretto, T., Abbadi, M., Biasini, L., Toffan, A., & Mezali, K. (2020). Viral encephalopathy and retinopathy is endemic in wild groupers (genus Epinephelus spp.) of the Algerian coast. Journal of Fish Diseases, 43(7), 801 812. https://doi.org/10.1111/jfd.13181
Bovo, G., Gustinelli, A., Quaglio, F., Gobbo, F., Panzarin, V., Fusaro, A., Mutinelli, F., Caffara, M., & Fioravanti, M.L. (2011). Viral encephalopathy and retinopathy outbreak in freshwater fish farmed in Italy. Diseases of Aquatic Organisms, 96(1), 45–54. https://doi.org/10.3354/dao02367

Chi, S.C., Shieh, J.R., & Lin, S.J. (2003). Genetic and antigenic analysis of betanodaviruses isolated from aquatic organisms in Taiwan. Diseases of Aquatic Organisms, 55(3), 221–228. https://doi.org/10.3354/dao055221
Chen, N.C., Yoshimura, M., Guan, H.H., Wang, T.Y., Misumi, Y., Lin, C.C., Chuankhayan, P., Nakagawa, A., Chan, S.I., Tsukihara, T., Chen, T.Y., & Chen, C.J. (2015). Crystal structures of a piscine betanodavirus: Mechanisms of capsid assembly and viral infection. PLoS pathogens, 11(10), e1005203. https://doi.org/10.1371/journal.ppat.1005203
Costa, J.Z., & Thompson, K.D. (2016). Understanding the interaction between betanodavirus and its host for the development of prophylactic measures for viral encephalopathy and retinopathy. Fish & Shellfish Immunology, 53, 35–49. https://doi.org/10.1016/j.fsi.2016.03.033
Çiçek, E., Sungur, S., & Fricke, R. (2020). Freshwater lampreys and fishes of Turkey: A revised and updated annotated checklist 2020. Zootaxa, 4809(2), 241–270. https://doi.org/10.11646/zootaxa.4809.2.2
Eren, H., Kaplan, M., & Yavru, S. (2024). The current status of viral nervous necrosis disease in Türkiye. Journal of Limnology and Freshwater Fisheries Research, 10(2), 134 142. https://doi.org/10.17216/limnofish.1449488
Fernández-Sánchez, J.L., Breton, A.L., Brun, E., Vendramin, N., Spiliopoulos, G., Furones, D., & Basurco, B. (2022). Assessing the economic impact of diseases in Mediterranean grow-out farms culturing European sea bass. Aquaculture, 547, Article 737530. https://doi.org/10.1016/j.aquaculture.2021.737530
Frerichs, G.N., Tweedie, A., Starkey, W.G., & Richards, R.H. (2000). Temperature, pH and electrolyte sensitivity, and heat, UV and disinfectant inactivation of sea bass (Dicentrarchus labrax) neuropathy nodavirus. Aquaculture, 185(1–2), 13–24. https://doi.org/10.1016/S0044-8486(99)00337-3
Galil, B.S., Boero, F., Campbell, M.L., Carlton, J.T., Cook, E., Fraschetti, S., Gollasch, S., Hewitt, C.L., Jelmert, A., Macpherson, E., Marchini, A., McKenzie, C.H., Minchin, D., Occhipinti-Ambrogi, A., Ojaveer, H., Olenin, S., Piraino, S., & Ruiz, G.M. (2015). ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biological Invasions, 17(4), 973–976. https://doi.org/10.1007/s10530-014-0778-y
Gherbawy, Y.A., Thabet, M.A., & Sultan, S. (2024). Genetic and morphological characterization of a new genotype of nervous necrosis virus circulating among Nile tilapia in the south of Egypt. International Microbiology, 27, 559–569. https://doi.org/10.1007/s10123-023-00406-5
Gomez, D.K., Lim, D.J., Baeck, G.W., Youn, H.J., Shin, N.S., Youn, H.Y., Hwang, C.Y., Park, J.H., & Park, S.C. (2006). Detection of betanodaviruses in apparently healthy aquarium fishes and invertebrates. Journal of Veterinary Science, 7(4), 369 374. https://doi.org/10.4142/jvs.2006.7.4.369
Gomez, D.K., Baeck, G.W., Kim, J.H., Choresca, C.H., Jr., & Park, S.C. (2008). Molecular detection of betanodaviruses from apparently healthy wild marine invertebrates. Journal of Invertebrate Pathology, 97(3), 197–202. https://doi.org/10.1016/j.jip.2007.10.012
Gomez, D.K., Mori, K.I., Okinaka, Y., Nakai, T., & Park, S.C. (2010). Trash fish can be a source of betanodaviruses for cultured marine fish. Aquaculture, 302(3 4), 158 163. https://doi.org/10.1016/j.aquaculture.2010.02.033
Harwood, M., South, J., Dunn, A.M., Stebbing, P.D., Burgess, A., & Bojko, J. (2025). Pathogen diversity of the non-native narrow-clawed crayfish (Pontastacus leptodactylus) in a UK water body. Journal of Invertebrate Pathology, 214, 108458. https://doi.org/10.1016/j.jip.2025.108458
Kalaycı, G., Özkan, B., Pekmez, K., & Kaplan, M. (2016). Levrek ve çipura kuluçkahanelerinde viral nervöz nekrozis hastalığının durumu. In XII. Veteriner Hekimleri Mikrobiyoloji Kongresi (Kapadokya, Nevşehir, Türkiye, 30 August – 2 September 2016).
Kalıpcı, E., Başer, V., Türkmen, M., Genç, N., & Cüce, H. (2021). Türkiye kıyılarında deniz suyu sıcaklık değişiminin CBS ile analizi ve ekolojik etkilerinin değerlendirilmesi. Doğal Afetler ve Çevre Dergisi, 7(2), 278–288. https://doi.org/10.21324/dacd.829938
Kaplan, M., & Karaoğlu, M.T. (2021). Investigation of betanodavirus in sea bass (Dicentrarchus labrax) at all production stages in all hatcheries and on selected farms in Turkey. Archives of Virology, 166(12), 3343–3356. https://doi.org/10.1007/s00705-021-05254-0
Kaplan, M., Pekmez, K., Özkan, B., Çağırgan, A.A., & Kalaycı, G. (2021). Detection of RGNNV genotype betanodavirus in the Black Sea and monitoring studies. Diseases of Aquatic Organisms, 144, 117–121. https://doi.org/10.3354/dao03583
Kaplan, M., Pekmez, K., Cagirgan, A.A., Arslan, F., Özkan, B., & Kalaycı, G. (2022a). The first detection of betanodavirus reassortant genotype (RGNNV/SJNNV) isolated from gilthead sea bream (Sparus aurata) in the Turkish coastlines: The importance of screening and monitoring studies for identifying the source of the infection. Journal of Fish Diseases, 45(6), 783–793. https://doi.org/10.1111/jfd.13603
Kaplan, M., Pekmez, K., Çağırgan, A.A., Özkan, B., Arslan, F., Kafa, B., & Kalaycı, G. (2022b). Türkiye’de çift kabuklu yumuşakçalarda Betanodavirus varlığının araştırılması. Acta Aquatica Turcica, 18(3), 415-425. https://doi.org/10.22392/actaquatr.1088276
Kaplan, M., Pekmez, K., Çağırgan, A.A., Tekelioğlu, B.K., Oğuz, U., Kafa, B., Arslan, F., & Kalaycı, G. (2023). Survey on Betanodavirus in wild fish species in the Turkish coastlines of the Mediterranean Sea and molecular characterization: Detecting different genotypes from different fish in different locations. Bulletin of the European Association of Fish Pathologists, 43(2), 73–92. https://doi.org/10.48045/001c.74914
Kim, K.I., Kwon, W.J., Kim, Y.C., Kim, M.S., Hong, S., & Jeong, H.D. (2016). Surveillance of aquatic animal viruses in seawater and shellfish in Korea. Aquaculture, 461, 17 24. https://doi.org/10.1016/j.aquaculture.2016.03.053
KOSKS. (2024). Kış Ortası Su Kuşu Sayım Raporu. Retrieved December 8, 2024, from https://www.tarimorman.gov.tr/DKMP/Belgeler/D%C4%B0%C4%9EER%20DUYURU/KOSKS_Raporu_2024.pdf
Kuo, H.C., Wang, T.Y., Hsu, H.H., Chen, P.P., Lee, S.H., Chen, Y.M., Tsai, T.J., Wang, C.K., Ku, H.T., Lee, G.B., & Chen, T.Y. (2012). Nervous necrosis virus replicates following the embryo development and dual infection with iridovirus at juvenile stage in grouper. PloS One, 7(4), e36183. https://doi.org/10.1371/journal.pone.0036183
Mori, K., Nakai, T., Muroga, K., Arimoto, M., Mushiake, K., & Furusawa, I. (1992). Properties of a new virus belonging to Nodaviridae found in larval striped jack (Pseudocaranx dentex) with nervous necrosis. Virology, 187(1), 368–371. https://doi.org/10.1016/0042-6822(92)90329-n
Munday, B.L., Kwang, J., & Moody, N. (2002). Betanodavirus infections of teleost fish: A review. Journal of Fish Diseases, 25(3), 127–142. https://doi.org/10.1046/j.1365-2761.2002.00350.x Müftüoğlu, B. (2023). Epidemiology of Betanodavirus infection in captured fish in the Black Sea. Doctoral dissertation, Ondokuz Mayıs University, Türkiye.
Nishizawa, T., Furuhashi, M., Nagai, T., Nakai, T., & Muroga, K. (1997). Genomic classification of fish nodaviruses by molecular phylogenetic analysis of the coat protein gene. Applied and Environmental Microbiology, 63(4), 1633–1636. https://doi.org/10.1128/aem.63.4.1633-1636.1997
Oğuz, U., Kaplan, M., & Kalaycı, G. (2023). Koi (Cyprinus carpio) ve Japon balıklarında (Carassius auratus) betanodavirus varlığının araştırılması. Journal of Limnology and Freshwater Fisheries Research, 9(1), 37-42. https://doi.org/10.17216/limnofish.1141342
Oğuz, U. (2024). Investigation of viral nervous necrosis (VNN) virus in sea bass (Dicentrarchus labrax), sea bream (Sparus aurata), and some mullet species (Mugil spp.) in lagoons in the Mediterranean Region (Akyatan, Akgöl-Paradeniz, and Beymelek). Doctoral dissertation, Selçuk University, Türkiye.
Olveira, J.G., Souto, S., Dopazo, C.P., Thiéry, R., Barja, J.L., & Bandín, I. (2009). Comparative analysis of both genomic segments of betanodaviruses isolated from epizootic outbreaks in farmed fish species provides evidence for genetic reassortment. Journal of General Virology, 90(Pt 12), 2940–2951. https://doi.org/10.1099/vir.0.013912-0
Olveira, J.G., Souto, S., Bandín, I., & Dopazo, C.P. (2021). development and validation of a SYBR green real time PCR protocol for detection and quantification of nervous necrosis virus (NNV) using different standards. Animals, 11(4), 1100. https://doi.org/10.3390/ani11041100
Özkan Özyer, B., Kalaycı, G., İnçoğlu, Ş., Pekmez, K., & Küçükali, Y. (2014). Türkiye’de kültürü yapılan levreklerden Betanodavirus’un ilk izolasyonu. Bornova Veteriner Bilimleri Dergisi, 36(50), 13–17.
Padrós, F., Caggiano, M., Toffan, A., Constenla, M., Zarza, C., & Ciulli, S. (2022). Integrated management strategies for viral nervous necrosis (VNN) disease control in marine fish farming in the Mediterranean. Pathogens, 11(3), 330. https://doi.org/10.3390/pathogens11030330
Panzarin, V., Patarnello, P., Mori, A., Rampazzo, E., Cappellozza, E., Bovo, G., & Cattoli, G. (2010). Development and validation of a real-time TaqMan PCR assay for the detection of betanodavirus in clinical specimens. Archives of Virology, 155(8), 1193–1203. https://doi.org/10.1007/s00705-010-0701-5
Panzarin, V., Fusaro, A., Monne, I., Cappellozza, E., Patarnello, P., Bovo, G., Capua, I., Holmes, E.C., & Cattoli, G. (2012). Molecular epidemiology and evolutionary dynamics of betanodavirus in southern Europe. Infection, Genetics and Evolution, 12(1), 63 70. https://doi.org/10.1016/j.meegid.2011.10.007
Panzarin, V., Cappellozza, E., Mancin, M., Milani, A., Toffan, A., Terregino, C., & Cattoli, G. (2014). In vitro study of the replication capacity of the RGNNV and the SJNNV betanodavirus genotypes and their natural reassortants in response to temperature. Veterinary Research, 45(1), 56. https://doi.org/10.1186/1297-9716-45-56
Praveenraj, J., Ezhil Praveena, P., Bhuvaneswari, T.V., Navaneeth Krishnan, A., & Jithendran, K. P. (2018). Experimental infection of betanodavirus in freshwater fish Gambusia affinis (Baird and Girard, 1853) A potential infection model for viral encephalopathy and retinopathy. Aquaculture International, 26, 617–627. https://doi.org/10.1007/s10499-018-0241-7
Sahul Hameed, A.S., Ninawe, A.S., Nakai, T., Chi, S.C., Johnson, K.L., & ICTV Report Consortium. (2019). ICTV Virus taxonomy profile: Nodaviridae. The Journal of General Virology, 100(1), 3–4. https://doi.org/10.1099/jgv.0.001170
Toffan, A., Pascoli, F., Pretto, T., Panzarin, V., Abbadi, M., Buratin, A., Quartesan, R., Gijón, D., & Padrós, F. (2017). Viral nervous necrosis in gilthead sea bream (Sparus aurata) caused by reassortant betanodavirus RGNNV/SJNNV: An emerging threat for Mediterranean aquaculture. Scientific Reports, 7, Article 46755. https://doi.org/10.1038/srep46755
Valero, Y., & Cuesta, A. (2023). Reassortant viruses threatening fish aquaculture. Reviews in Aquaculture, 15(4): 1720-1731. https://doi.org/10.1111/raq.12813
Vázquez-Salgado, L., Olveira, J.G., Dopazo, C.P., & Bandín, I. (2024). Detection of different betanodavirus genotypes in wild fish from Spanish Atlantic coastal waters (Galicia, northwestern Spain). Journal of Aquatic Animal Health, 36(1), 57–69. https://doi.org/10.1002/aah.10201
Vendramin, N., Padrós, F., Pretto, T., Cappellozza, E., Panzarin, V., Bovo, G., Toffan, A., & Terregino, C. (2012). Viral encephalopathy and retinopathy outbreak in restocking facilities of the endangered freshwater species, Salaria fluviatilis (Asso). Journal of Fish Diseases, 35(11), 867–871. https://doi.org/10.1111/j.1365-2761.2012.01429.x
Volpe, E., Grodzki, M., Panzarin, V., Guercio, A., Purpari, G., Serratore, P., & Ciulli, S. (2018). Detection and molecular characterization of betanodaviruses retrieved from bivalve molluscs. Journal of Fish Diseases, 41(4), 603–611. https://doi.org/10.1111/jfd.12759
World Organisation for Animal Health (WOAH). (2019). Viral encephalopathy and retinopathy. In Manual of diagnostic tests for aquatic animals (Chapter 2.3.12). Retrieved from https://www.woah.org/en/what-we-do/standards/codes-and-manuals/aquatic-manual-online-access/
Xylouri, E., Kotzamanis, Y.R., Athanassopoulou, F., Dong, L., Pappas, L.S., Argyrokastritis, A., & Fragkiadaki, E. (2007). Isolation, characterization, and sequencing of nodavirus in sturgeon (Acipenser gueldestaedi L.) reared in freshwater facilities. The Israeli Journal of Aquaculture – Bamidgeh, 59(1), 36–41.
Yoğurtçuoğlu, B., & Ekmekçi, F.G. (2018). First record of the giant pangasius, Pangasius sanitwongsei (Actinopterygii: Siluriformes: Pangasiidae), from central Anatolia, Turkey. Acta Ichthyologica et Piscatoria, 48(3), 241–244. https://doi.org/10.3750/AIEP/02407
Ziarati, M., Zorriehzahra, M.J., Kafilzadeh, F., & Kargar, M. (2020). Molecular monitoring and phylogenetic analysis of betanodavirus in groupers (Epinephelus spp.) and Asian Sea bass (Lates calcarifer) of Iranian Northern Waters of the Persian Gulf. Current Microbiology, 77(12), 3919–3926. https://doi.org/10.1007/s00284-020-02222-w
Zrnčić, S., Brnić, D., Panzarin, V., Abbadi, M., Lojkić, I., Zupičić, I.G., & Oraić, D. (2022). Transmission pathways of the VNN introduced in Croatian marine aquaculture. Pathogens, 11(4), 418. https://doi.org/10.3390/pathogens11040418
Zrnčić S., Vendramin N., Boutrup T.S., Boye, M., Madsen, L., Nonneman, B., Brnić, D., & Oraić, D. (2021). First description and diagnostics of disease caused by Piscirickettsia salmonis in farmed European sea bass (Dicentrarchus labrax Linnaeus) from Croatia. Journal of Fish Diseases, 44(7), 1033–1042. https://doi.org/10.1111/jfd.13366

Ayrıntılar

Birincil Dil

İngilizce

Konular

Balık Zararlıları ve Hastalıkları

Bölüm

Araştırma Makalesi

Yazarlar

Hakan Eren ^*
0000-0001-8475-4237
Türkiye

Sibel Yavru
0000-0002-5839-364X
Türkiye

Yayımlanma Tarihi

13 Şubat 2026

Gönderilme Tarihi

6 Ekim 2025

Kabul Tarihi

9 Kasım 2025

Yayımlandığı Sayı

Yıl 1970 Cilt: 43 Sayı: 1

DOI

https://doi.org/10.12714/egejfas.43.1.01

IZ

https://izlik.org/JA33UE33RN

Kaynak Göster

RIS / Bibtex

APA

Eren, H., & Yavru, S. (2026). Investigation of the presence of nervous necrosis virus (NNV) in pikeperch (Sander lucioperca) and crayfish (Pontastacus leptodactylus). Ege Journal of Fisheries and Aquatic Sciences, 43(1), 1-8. https://doi.org/10.12714/egejfas.43.1.01

Sudak (Sander lucioperca) ve kerevitte (Pontastacus leptodactylus) nervöz nekrozis virüsünün (NNV) varlığının araştırılması

Sudak (Sander lucioperca) ve kerevitte (Pontastacus leptodactylus) nervöz nekrozis virüsünün (NNV) varlığının araştırılması

Öz

Anahtar Kelimeler