Epizootic situation of bacterial kidney disease (BKD)

Relevance. Bacterial kidney disease (BKD, corineal renal infection, Di disease), the causative agent of which is the gram–positive non-spore motionless bacterium Renibacterium salmoninarum, is a common disease of salmon fish (Salmonidae), which causes significant damage to fish production in aquaculture and the development of the industry, as well as reduces the number of wild populations.

The purpose of this review was to analyze the epizootic situation of bacterial renal disease (BKD) among wild salmon and fish populations in aquaculture on the territory of the Russian Federation, as well as in other countries.

The article presents information on the incidence of BKD in the world and on the territory of the Russian Federation for the period 1933–2023, shows data on the spread of the disease among wild populations and farmed fish in aquaculture, describes possible transmission routes, native and suspected vectors of infection.

Methods. The authors consider measures to control the growth of the incidence of BKD in the world and on the territory of the Russian Federation. Due to the lack of an effective vaccine and a method of treatment, the most affordable method of controlling the spread of the disease is timely diagnosis. The article describes the methods developed for fast and effective diagnostics by the staff of the Laboratory of Ichthyopathology of the FSC VIEV: microagglutination reaction (PMA) and polymerase chain reaction in real time (real-time PCR).

Results. Unlike classical bacteriological methods, these reactions allow for the indication and identification of the causative agent of BKD within 24 hours.

1. Droshnev A.E., Bulina K.Y., Alontseva D.A., Belimenko V.V., Zavyalova E.A. Microbiological monitoring of causative agents of infectious diseases of salmons in the Northwest region. IOP Conference Series: Earth and Environmental Science. 2019; 315(7): 72007. https://doi.org/10.1088/1755-1315/315/7/072007

2. Evelyn T.P.T. Bacterial Kidney Disease – BKD. Inglis V., Roberts R.J., Bromage N.R. (eds.). Bacterial Diseases of Fish. Oxford, UK: Blackwell Scientific Publications. 1993; 177–195.

3. Rahkonen R., Wennerstrom P., Rintamaki P., Kannel R. Healthy fish-pre-vention, diagnosis and treatment of the disease. 2nd ed. Helsinki: Finnish Game and Fisheries Research Institute. 2013; 177 (In Russian). ISBN 978-951-776-935-8

4. Mackie T.J., Arkwright J.A., Pryce-Tannatt T.E., Mottram J.C., Johnston W.P., Menzies W.J.M. Second Interim Report of the Furunculosis Committee. Edinburgh: HMSO. 1933; 81.

5. Belding D.L., Merrill B. A Preliminary Report upon a Hatchery Disease of the Salmonidae. Transactions of the American Fisheries Society. 1935; 65(1): 76–84. https://doi.org/10.1577/1548-8659(1935)65[76:APRUAH]2.0.CO;2

6. Rucker R.R., Earp B.J., Ordal E.J. Infectious Diseases of Pacific Salmon. Transactions of the American Fisheries Society. 1954; 83(1): 297–312. https://doi.org/10.1577/1548-8659(1953)83[297:IDOPS]2.0.CO;2

7. Ordal E.J., Earp B.J. Cultivation and Transmission of Etiological Agent of Kidney Disease in Salmonid Fishes. Proceedings of the Society for Experimental Biology and Medicine. 1956; 92(1): 85–88. https://doi.org/10.3181/00379727-92-2239

8. Balfry S.K., Albright L.J., Evelyn T.P.T. Horizontal transfer of Renibacterium salmoninarum among farmed salmonids via the fecal-oral route. Diseases of Aquatic Organisms. 1996; 25(1–2): 63–69. https://doi.org/10.3354/dao025063

9. Bruno D.W. Prevalence and diagnosis of bacterial kidney disease (BKD) in Scotland between 1990 and 2002. Diseases of Aquatic Organisms. 2004; 59(2): 125–130. https://doi.org/10.3354/dao059125

10. Johansen L.-H., Jensen I., Mikkelsen H., Bjørn P.-A., Jansen P.A., Bergh Ø. Disease interaction and pathogens exchange between wild and farmed fish populations with special reference to Norway. Aquaculture. 2011; 315(3–4): 167–186. https://doi.org/10.1016/j.aquaculture.2011.02.014

11. Boerlage A.S., Stryhn H., Sanchez J., Hammell K.L. Case definition for clinical and subclinical bacterial kidney disease (BKD) in Atlantic Salmon (Salmo salar L.) in New Brunswick, Canada. Journal of Fish Diseases. 2017; 40(3): 395–409. https://doi.org/10.1111/jfd.12521

12. Jónsdóttir H., Malmquist H.J., Snorrason S.S., Gudbergsson G., Gudmundsdóttir S. Epidemiology of Renibacterium salmoninarum in wild Arctic charr and brown trout in Iceland. Journal of Fish Biology. 1998; 53(2): 322–339. https://doi.org/10.1111/j.1095-8649.1998.tb00984.x

13. Suzuki K., Misaka N., Mizuno S., Sasaki Y. Subclinical Infection of Renibacterium salmoninarum in Fry and Juveniles Chum Salmon Oncorhynchus keta in Hokkaido, Japan. Fish Pathology. 2017; 52(2): 89–95. https://doi.org/10.3147/JSFP.52.89

14. Du Y., Hu X., Miao L., Chen J. Current status and development prospects of aquatic vaccines. Frontiers in Immunology. 2022; 13: 1040336. https://doi.org/10.3389/fimmu.2022.1040336

15. Bruneau N.N., Thorburn M.A., Stevenson R.M.W. Occurrence of Aeromonas salmonicida, Renibacterium salmoninarum, and Infectious Pancreatic Necrosis Virus in Ontario Salmonid Populations. Journal of Aquatic Animal Health. 1999; 11(4): 350–357. https://doi.org/10.1577/1548-8667(1999)011<0350:ooasrs>2.0.co;2

16. Alontseva D.A., Zavyalova E.A., Droshnev A.E., Bulina K.Yu. Screening of bacterial kidney disease in the North-West region of the Russian Federation. IOP Conference Series: Earth and Environmental Science. 2021; 677: 052092. https://doi.org/10.1088/1755-1315/677/5/052092

17. Fryer J.L., Sanders J.E. Bacterial kidney disease of salmonid fish. Annual Review of Microbiology. 1995; 35: 273–298. https://doi.org/10.1146/annurev.mi.35.100181.001421

18. Pfeil-Putzien C., Hoffmann R., Popp W. Preliminary report on the occurrence of bacterial kidney disease in Germany. Bulletin of the European Association of Fish Pathologists. 1985; 5(2): 30–31.

19. Kettler S., Pfeil-Putzien C., Hoffmann R. Infection of grayling (Thymallus thymallus) with the agent of bacterial kidney disease (BKD). Bulletin of the European Association of Fish Pathologists. 1986; 6(3): 69–71.

20. Nagai T., Iida Y. Occurrence of Bacterial Kidney Disease in Cultured Ayu. Fish Pathology. 2002; 37(2): 77–81. https://doi.org/10.3147/jsfp.37.77

21. Rimaila-Pärnänen E. First case of bacterial kidney disease (BKD) in whitefish (Coregonus lavaretus) in Finland. Bulletin of the European Association of Fish Pathologists. 2002; 22(6): 403–404.

22. Bell G.R., Hoffmann R.W., Brown L.L. Pathology of experimental infections of the sablefish, Anoplopoma fimbria (Pallas), with Renibacterium salmoninarum, the agent of bacterial kidney disease in salmonids. Journal of Fish Diseases. 1990; 13(5): 355–367. https://doi.org/10.1111/j.1365-2761.1990.tb00794.x

23. Sakai M., Ogasawara K., Atsuta S., Kobayashi M. Comparative sensitivity of carp, Cyprinus carpio L. and rainbow trout, Salmo gairdneri Richardson, to Renibacterium salmoninarum. Journal of Fish Diseases. 1989; 12(4): 367–372. https://doi.org/10.1111/j.1365-2761.1989.tb00325.x

24. Bell G.R., Traxler G.S. Resistance of Pacific lamprey, Lampetra tridentata (Gairdner), to challenge by Renibacterium salmoninarum, the causative agent of kidney disease in salmonids. Journal of Fish Diseases. 1986; 9(3): 277–279. https://doi.org/10.1111/j.1365-2761.1986.tb01014.x

25. Paclibare J.O., Evelyn T.P.T., Albright L.J., Prosperi-Porta L. Clearing of the kidney disease bacterium Renibacterium salmoninarum from seawater by the blue mussel Mytilus edulis, and the status of the mussel as a reservoir of the bacterium. Diseases of Aquatic Organisms. 1994; 18(2): 129–133. https://doi.org/10.3354/dao018129

26. Starliper C.E., Morrison P. Bacterial pathogen contagion studies among freshwater bivalves and salmonid fishes. Journal of Shellfish Research. 2000; 19(1): 251–258.

27. Faisal M. et al. Epidemiological investigation of Renibacterium salmoninarum in three Oncorhynchus spp. in Michigan from 2001 to 2010. Preventive Veterinary Medicine. 2012; 107(3–4): 260–274. https://doi.org/10.1016/j.prevetmed.2012.06.003

28. Murray A.G., Munro L.A., Wallace I.S., Allan C.E.T., Peeler E.J., Thrush M.A. Epidemiology of Renibacterium salmoninarum in Scotland and the potential for compartmentalised management of salmon and trout farming areas. Aquaculture. 2012; 324–328: 1–13. https://doi.org/10.1016/j.aquaculture.2011.09.034

29. Lorenzen E., Olesen N.J., Korsholm H., Heuer O.E., Evensen Ø. First demonstration of Renibacterium salmoninarum / BKD in Denmark. Bulletin of the European Association of Fish Pathologists. 1998; 17(3–4): 140–144.

30. Pedersen K., Skall H.F., Lassen-Nielsen A.M., Nielsen T.F., Henriksen N.H., Olesen N.J. Surveillance of health status on eight marine rainbow trout, Oncorhynchus mykiss (Walbaum), farms in Denmark in 2006. Journal of Fish Diseases. 2008; 31(9): 659–667. https://doi.org/10.1111/j.1365-2761.2008.00941.x

31. Delghandi M.R., Menanteau-Ledouble S., Waldner K., El-Matbouli M. Renibacterium salmoninarum and Mycobacterium spp.: two bacterial pathogens present at low levels in wildbrown trout (Salmo trutta fario) populations in Austrian rivers. BMC Veterinary Research. 2020; 16: 40. https://doi.org/10.1186/s12917-020-2260-7

32. Mora-Salas P. et al. Method for lineage typing of epidemic Renibacterium salmoninarum in Chilean salmon farms. Journal of Fish Diseases. 2023; 46(5): 499–506. https://doi.org/10.1111/jfd.13761

33. Bayliss S.C. et al. Genomic epidemiology of the commercially important pathogen Renibacterium salmoninarum within the Chilean salmon industry. Microbial Genomics. 2018; 4(9). https://doi.org/10.1099/mgen.0.000201

34. Sakai M., Atsuta S., Kobayashi M. Susceptibility of Five Salmonid Fishes to Renibacterium salmoninarum. Fish Pathology. 1991; 26(3): 159–160. https://doi.org/10.3147/jsfp.26.159

35. Matsui T., Nishizawa T., Yoshimizu M. Modification of KDM-2 with Culture-spent Medium for Isolation of Renibacterium salmoninarum. Fish Pathology. 2009; 44(3): 139–144. https://doi.org/10.3147/jsfp.44.139

36. Suzuki K., Misaka N., Mizuno S., Sasaki Y. Subclinical Infection of Renibacterium salmoninarum in Fry and Juveniles Chum Salmon Oncorhynchus keta in Hokkaido, Japan. Fish Pathology. 2017; 52(2): 89–95. https://doi.org/10.3147/jsfp.52.89

37. Suzuki K., Mizuno S., Katsumata Y., Misaka N., Miyamoto M., Sasaki Y. Asymptomatic Infection of Renibacterium salmoninarum in Hatchery-reared Juvenile Chum Salmon Oncorhynchus keta Resulted in Mass Mortalities after Long-term Rearing. Fish Pathology. 2018; 53(1): 40–43. https://doi.org/10.3147/jsfp.53.40

38. Yoshimizu M. Disease problems of salmonid fish in Japan caused by international trade. Revue Scientifique et Technique. 1996; 15(2): 533–549. https://doi.org/10.20506/rst.15.2.937

39. Rudakova S.L. The science-based approach for maintenance of aquatic animal health security of Russian aquaculture. Trudy VNIRO. 2016; 162: 104–115 (In Russian). https://elibrary.ru/xagkmn

40. Zavyalova E.A., Droshnev A.E., Alontseva D.A., Bulina Ch.Yu., Karpova M.A. Detection of Renibacterium salmoninarum in salmon fish using molecular genetic and bacterial methods. Veterinary medicine. 2023; (5): 24–31 (In Russian). https://doi.org/10.30896/0042-4846.2023.26.5.24-30

41. Sergeenko N.V., Ustimenko E.A., Eliseikina M.G., Kuhlevskiy A.D., Bochkova E.V., Ryazanova T.V. First report of bacterial kidney disease in coho salmon Oncorhynchus kisutch in Russia. Diseases of aquatic organisms. 2020; 140: 31–36. https://doi.org/10.3354/dao03486

42. Salonius K., Siderakis C., MacKinon A. M., Griffiths S. G. Use of Arthrobacter davidanieli as a live vaccine against Renibacterium salmoninarum and Piscirickettsia salmonis in salmonids. Developments in Biologicals. 2005; 121:189-197.

43. Alcorn S., Murray A. L., Pascho R. J., Varney J. A cohabitation challenge to compare the efficacies of vaccines for bacterial kidney disease (BKD) in chinook salmon Oncorhynchus tshawytscha. Dis Aquat Org. 2005; 63:151-160.

44. Evelyn T.P.T. An improved growth medium for the kidney disease bacterium and some notes on using the medium. Bulletin de L’Office International des Epizooties. 1977; 87:511–513.

45. Austin B., Embly T. M., Goodfellow M. Selective isolation of Renibactenum salmonlnarum. FEMS Microblol Lett. 1983; 17:111-114.

46. Bandin I., Heinen P., Brown L.L., Toranzo A.E. Comparison of different ELISA kits for detecting Renibacterium salmoninarum. Bulletin of the European Association of Fish Pathologists. 1996; 16:19–22.

47. Chase D.M., Pascho R. J. Development of a nested polymerase chain reaction for amplification of a sequence of the p57 gene of Renibacterium salmoninarum that provides a highly sensitive method for detection of the bacterium in salmonid kidney. Dis Aquat Org. 1998;34:223–229

48. Chase D.M., Elliot D.G., Pascho R.J. Detection and quantification of Renibacterium salmoninarum DNA in salmonid tissues by real-time quantitative polymerase chain reaction analysis. J Vet Diagn Invest. 2006; 18:375–380.

49. Halaihel N. et al. A new real time PCR-based assay for diagnosing Renibacterium salmoninarum in rainbow trout (Oncorhynchus mykiss) and comparison with other techniques. Journal of Microbiological Methods. 2009; 6:75–80.

50. Etchegaray J.P., Martinez M.A., Krauskopf M., Leon, G. Molecular cloning of Renibacterium salmoninarum DNA fragments. FEMS Microbiology Letters. 1991; 79:61–64.

51. Alontseva D.A., Zavyalova E.A., Droshnev A.E., Karpova M.A., Bulina K.Yu. Development of a symptom complex in rabbits when receiving antiserum against the causative agent of bacterial kidney disease of salmonids (BKD). Veterinary, Zootechnics and Biotechnology. 2022; (2): 21–28 (In Russian). https://doi.org/10.36871/vet.zoo.bio.202202003

52. Alontseva D.A., Droshnev A.E., Zavyalova E.A. Development of real-time PCR for detection and identification of the causative agent of Bacterial Kidney Disease of salmon fish. Veterinary, Zootechnics and Biotechnology. 2023; (7): 34–41 (In Russian). https://doi.org/10.36871/vet.zoo.bio.202307004