Advertisement

Outbreak of carp edema virus disease in cultured ornamental koi in a lower temperature in China

  • Ping Ouyang
  • Yaojia Zhou
  • Ruixue Yang
  • Zhuangzhi Yang
  • Kaiyu Wang
  • Yi Geng
  • Weiming Lai
  • Xiaoli Huang
  • Defang Chen
  • Jing Fang
  • Zhengli Chen
  • Li Tang
  • Chao Huang
  • Lizi YinEmail author
Article
  • 4 Downloads

Abstract

Carp edema virus (CEV) is the pathogen of carp edema virus disease (CEVD), an emerging infectious disease with high morbidity and mortality worldwide. In the winter of 2016, a disease outbreak occurred in a koi pond in Chengdu, located in the southwest of China. The water temperature at that time was 11–13 °C. The clinical signs of the diseased koi were lethargy, unresponsiveness, enophthalmos, swollen gills, and hemorrhagic skin. Histopathological changes were observed in moribund fish, such as significant cell hyperplasia in the gill lamellae, and swelling and vacuolar degeneration in epithelial cells of the renal tubules and hepatocytes. Electron microscopy of renal tissues showed virions of a pox-like virus (200–235 nm diameter). The presence of specific 528 bp and 478 bp fragments was detected by nested PCR. An experimental infection demonstrated cumulative mortality of 15% (3/20) at a water temperature of 13 ± 2 °C. Furthermore, sequence analysis of the partial 4a genes showed that the CEV isolate (MG189372) in this study had 100% homology with a UK strain (KX254027). The evidence showed that the pathogen involved in this outbreak was CEV. To the best of our knowledge, this is the first report of carp disease caused by CEV at low temperature in China, demonstrating that CEV disease should be monitored in the cold season and at low temperatures. The findings are of profound significance to reducing the risk of CEVD outbreaks in carp aquaculture.

Keywords

Carp edema virus (CEV) Koi sleep disease (KSD) Infectious disease Low temperature 

Notes

Acknowledgments

This work was supported by a project funded by the China Postdoctoral Science Foundation (2015M582563) and the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry (No. [2015]311).

Data availability statement

The authors confirm that the data supporting the findings of this study are available within the article.

Author contributions

K.W., Y.G., and L.Y. conceived and designed the experiments. P.O., Y. Z., and R.Y. performed the experiments. W.L. and X.H. contributed to the histopathology preparation. D.C. provided fish samples. C.H. and L.T. contributed the bioinformatics analysis. P.O., Y. Z., and R.Y. wrote the paper. J.F., Z.C., and L.Y. proofread the manuscript.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

References

  1. Adamek M, Jung-Schroers V, Hellmann J, Teitge F, Bergmann SM, Runge M, Steinhagen D (2016) Concentration of carp edema virus (CEV) DNA in koi tissues affected by koi sleepy disease (KSD). Dis Aquat Org 119(3):245.  https://doi.org/10.3354/dao02994 CrossRefPubMedGoogle Scholar
  2. Adamek M, Baska F, Vincze B, Steinhagen D, Adamek M, Baska F, Steinhagen D (2017a) Carp edema virus from three genogroups is present in common carp in Hungary. J Fish Dis 41(3):463–468.  https://doi.org/10.1111/jfd.12744 CrossRefPubMedGoogle Scholar
  3. Adamek M, Oschilewski A, Wohlsein P, Jungschroers V, Teitge F, Dawson A, Adamek J (2017b) Experimental infections of different carp strains with the carp edema virus (CEV) give insights into the infection biology of the virus and indicate possible solutions to problems caused by koi sleepy disease (KSD) in carp aquaculture. Vet Res 48(1):12–16.  https://doi.org/10.1186/s13567-017-0416-7 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Antynchowicz, J., Reichert, M., Matras, M., Bergmann, S.M., Haenen, O.L.M 2005 Epidemiology, pathogenicity and molecular biology of koi herpesvirus isolated in Poland. B VET I PULAWY, 49, 367–373.  https://doi.org/10.1111/j.1751-0813.2005.tb12210.x CrossRefGoogle Scholar
  5. Bachmann J, Keilholz S (2016) Frühjahrsverluste in der fränkischen Karpfenteichwirtschaft-Viraler Erreger als Ursache? Erstnachweise der KSD/CEV in Bayern. Fisch Teichwirt 3:91–92Google Scholar
  6. Boutier M, Ronsmans M, Rakus K, Jazowiecka-Rakus J, Vancsok C, Morvan L, Vanderplasschen A (2015) Cyprinid Herpesvirus 3. Adv Virus Res:161–256.  https://doi.org/10.1016/bs.aivir.2015.03.001 Google Scholar
  7. Haenen O, Way K, Stone D, Engelsma M (2014) ‘Koi sleepy disease’ found for the first time in koi carps in the Netherlands. Tijdschr Diergeneeskd 139(4):26PubMedGoogle Scholar
  8. Hedrick R, Antonio R, Munn D (1997) Poxvirus like agent associated with epizootic mortality in juvenile koi (Cyprinus carpio). FHS Newsletter 25:1–2Google Scholar
  9. Hesami, S., Viadanna, P., Steckler, N., Spears, S.,Thompson, P.,Kelley, K., Waltzek, T (2015) Carp edema virus disease (CEVD)/koi sleepy disease (KSD). EDIS Publication FA189. University of FloridaGoogle Scholar
  10. Jung-Schroers V, Adamek M, Teitge F, Hellmann J, Bergmann SM, Schütze H, Runge M (2015) Another potential carp killer? Carp edema virus disease in Germany. BMC Vet Res 11(1):114–114.  https://doi.org/10.1186/s12917-015-0424-7 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Kim, S.W., Jun, J.W., Giri, S.S., Chi, C., Yun, S., Kim, H.J., Park, S.C (2017) First report of carp oedema virus infection of koi (Cyprinus carpio haematopterus) in the Republic of Korea. Transbound Emerg Dis, 65(2).  https://doi.org/10.1111/tbed.12782 CrossRefGoogle Scholar
  12. Lewisch E, Gorgoglione B, Way K, El-Matbouli M (2015) Carp edema virus/koi sleepy disease: an emerging disease in central-East Europe. Transbound Emerg Dis 62(1):6–12.  https://doi.org/10.1111/tbed.12293 CrossRefPubMedGoogle Scholar
  13. Matras, M., Borzym, E., Stone, D., Way, K., Stachnik, M., Maj-Paluch, J., Reichert, M (2016) Carp edema virus in Polish aquaculture - evidence of significant sequence divergence and a new lineage in common carp Cyprinus carpio (L.). J Fish Dis, 40(3).  https://doi.org/10.1111/jfd.12518 CrossRefGoogle Scholar
  14. Miyazaki T, Isshiki T, Katsuyuki H (2005) Histopathological and electron microscopy studies on sleepy disease of koi Cyprinus carpio koi in Japan. Dis Aquat Org 65:197–207.  https://doi.org/10.3354/dao065197 CrossRefPubMedGoogle Scholar
  15. Ono SI, Nagai A, Sugai N (1986) A histopathological study on juvenile colorcarp, Cyprinus carpio, showing edema. Fish Pathol 21:167–175.  https://doi.org/10.3147/jsfp.21.167 CrossRefGoogle Scholar
  16. Ouyang P, Yang R, Chen J, Wang K, Geng Y, Lai W, Huang X, Chen D, Fang J, Chen Z (2018) First detection of carp edema virus in association with cyprinid herpesvirus 3 in cultured ornamental koi, Cyprinus carpio L., in China. Aquaculture 490:162–168.  https://doi.org/10.1016/j.aquaculture.2018.02.037 CrossRefGoogle Scholar
  17. Oyamatsu T, Hata N, Yamada K, Sano T, Fukuda H (1997) An etiological study on mass mortality of cultured color carp juveniles showing edema. Fish Pathol 32(2):81–88.  https://doi.org/10.3147/jsfp.32.81 CrossRefGoogle Scholar
  18. Pretto, T., Abbadi, M., Panzarin, V., Quartesan, R., Manfrin, A., Toffan, A (2015) Carp edema virus (CEV): first detection in Italy. In: 17th international conference on diseases of fish and shellfish, Las Palmas, Gran CanariaGoogle Scholar
  19. Swaminathan TR, Kumar R, Dharmaratnam A, Basheer VS, Sood N, Pradhan PK, Jena JK (2016) Emergence of carp edema virus in cultured ornamental koi carp, Cyprinus carpio koi, in India. J Gen Virol 97(12):3392.  https://doi.org/10.1099/jgv.0.000649 CrossRefPubMedGoogle Scholar
  20. Vesely, T., Pokorova, D., Reschova, S., Piackova, V (2015) Detection of carp edema virus in common carp (Cyprinus carpio) and koi in the Czech Republic. 17th International Conference on Diseases of Fish and Shellfsh. Las Palmas, Gran Canaria.Las Palmas, Gran Canaria Abstract and posterGoogle Scholar
  21. Viadanna, P., Pilarski, F., Hesami, S., Waltzek, T (2015) First report of carp edema virus (CEV) in south American koi. In: 40th Eastern Fish Health Workshop, Charleston, NC Abstract and presentationGoogle Scholar
  22. Viadanna PH, Millermorgan T, Peterson T, Way K, Stone DM, Marty GD, Waltzek TB (2017) Development of a PCR assay to detect cyprinid herpesvirus 1 in koi and common carp. Dis Aquat Org 123(1):19–27.  https://doi.org/10.3354/dao03066 CrossRefGoogle Scholar
  23. Way K, Stone D (2013) Emergence of carp edema virus-like (CEV-like) disease in the UK. In CEFAS Finfish News 15:32–34Google Scholar
  24. Way K, Haenen O, Stone D, Adamek M, Bergmann SM, Bigarrã L, Jung-Schroers V (2017) Emergence of carp edema virus (CEV) and its significance to European common carp and koi Cyprinus carpio. Dis Aquat Org 126(2):155–166.  https://doi.org/10.3354/dao03164 CrossRefGoogle Scholar
  25. Yuasa K, Kurita J, Kawana M, Kiryu I, Oseko N, Sano M (2012) Development of mRNA-specific RT-PCR for the detection of koi herpesvirus (KHV) replication stage. Dis Aquat Org 100(1):11–18.  https://doi.org/10.3354/dao02499 CrossRefGoogle Scholar
  26. Zhang X, Ni Y, Ye J, Xu H, Hou Y, Luo W, Shen W (2017) Carp edema virus, an emerging threat to the carp (Cyprinus carpio) industry in China. AQUACULTURE 474:34–39.  https://doi.org/10.1016/j.aquaculture.2017.03.033 CrossRefGoogle Scholar
  27. Zheng S, Wang Q, Yingying LI, Zeng W, Wang Y, Liu C, Shi C (2016) Research advances in cyprinid herpesvirus 3. Chinese Journal of Virology 32:108PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ping Ouyang
    • 1
  • Yaojia Zhou
    • 1
  • Ruixue Yang
    • 1
  • Zhuangzhi Yang
    • 2
  • Kaiyu Wang
    • 1
  • Yi Geng
    • 1
  • Weiming Lai
    • 1
  • Xiaoli Huang
    • 3
  • Defang Chen
    • 3
  • Jing Fang
    • 1
  • Zhengli Chen
    • 1
  • Li Tang
    • 1
  • Chao Huang
    • 1
  • Lizi Yin
    • 1
    Email author
  1. 1.Department of Basic Veterinary, College of Veterinary MedicineSichuan Agricultural UniversityChengduChina
  2. 2.Chengdu Academy of Agriculture and Forestry SciencesChengduChina
  3. 3.Department of Aquaculture, College of Animal Science and TechnologySichuan Agricultural UniversityChengduChina

Personalised recommendations