Advertisement

Streptococcosis in Oreochromis sp.: is feed-based biofilm vaccine of Streptococcus agalactiae effective?

  • M. Kahieshesfandiari
  • M. Y. SabriEmail author
  • M. Y. Ina-salwany
  • M. D. Hassan
  • O. Noraini
  • A. A. Ajadi
  • A. I. Isiaku
Article
  • 20 Downloads

Abstract

This study was carried out to determine the potential of a biofilm vaccine of Streptococcus agalactiae in protecting tilapia from streptococcocal infection. The tilapia were vaccinated orally using the biofilm vaccine with 1091010 CFU/g (FBV) incorporated in feed and killed whole-cell vaccine (FCV) of S. agalactiae also prepared in feed, and the unvaccinated control group (Cx) was fed with standard feed formulation. Throughout the study, serum, mucus and gut lavage fluid were collected to evaluate the antibody responses among the groups. The results showed that tilapia vaccinated with FBV exhibited significantly (p < 0.05) stronger immune response and high protection with the relative percentage survival (RPS) of more than 70% (85%) compared with the FCV group, which was only 56%. None of the tilapia in the Cx group survived (0%) post-challenge. Thus, the study revealed that the feed-based biofilm vaccine (FBV) significantly confers the immune protection against the high-dose challenge of S. agalactiae by secretion of the protective immunity in the mucosal and humoral in tilapia.

Keywords

Biofilm Streptococcus agalactiae Oreochromis sp. Oral vaccination 

Notes

Acknowledgement

We would like to thank the farmer involved in this study and staff of Aquaculture Experimental Station, Faculty of Agriculture, UPM, Puchong, Selangor, for their excellent technical assistance.

Funding information

This project was funded by the Ministry of Science, Technology and Innovation, Malaysia (MOSTI) under the vote no. 5450652.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional guidelines for the care and use of animals were followed by the authors.

References

  1. Agnew W, Barnes AC (2007) Streptococcus iniae: an aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination. Vet Microbiol 122(1):1–15CrossRefGoogle Scholar
  2. Alcamo IE (1997) Environment and industrial microbiology. Fundamentals of microbiology, 5th edn. Addison Wesley Longman, Inc, California, p 766Google Scholar
  3. Azad IS, Shankar KM, Mohan CV (1997) Evaluation of biofilm of Aeromonas hydrophila for oral vaccination of carps. Diseases in Asian aquaculture III. Fish Health Section, Asian Fisheries Society, Manila, pp 181–186Google Scholar
  4. Azad IS, Shankar KM, Mohan CV, Kalita B (1999) Biofilm vaccine of Aeromonas hydrophila standardization of dose and duration for oral vaccination of carps. Fish Shellfish Immunol 9(7):519–528CrossRefGoogle Scholar
  5. Azad IS, Shankar KM, Mohan CV, Kalita B (2000) Uptake and processing of biofilm and free-cell vaccines of Aeromonas hydrophila in Indian major carps and common carp following oral vaccination. Antigen localization by a monoclonal antibody. Dis Aquat Org 14:103–108CrossRefGoogle Scholar
  6. Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z (1997) Interactions between biofilms and the environment. FEMS Microbiol Rev 20:291–303CrossRefGoogle Scholar
  7. Campbell R, Adams A, Tatner MF, Chair M, Sorgeloos P (1993) Uptake of Vibrio anguillarum vaccine by Artemia salina as a potential oral delivery system to fish fry. Fish Shellfish Immunol 3:451–459CrossRefGoogle Scholar
  8. Dalmo R, Leifson RM, Bøgwald J (1995) Microspheres as antigen carriers: studies on intestinal absorption and tissue localization of polystyrene microspheres in Atlantic salmon, Salmo salar L. J Fish Dis 18(1):87–91CrossRefGoogle Scholar
  9. Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64(4):847–867CrossRefGoogle Scholar
  10. Davidson GA, Ellis AE, Secombes CJ (1993) Route of immunization influences the generation of antibody-secreting cells in the gut of rainbow trout (Oncorhynchus mykiss). Developmental and Comparative Immunology17, pp 373–376Google Scholar
  11. Effendy AW, Zamri-Saad M, Maswati MA, Ismail MS, Jamil SM (1998) Stimulation of the bronchus-associated lymphoid tissue of goats and its effect on in vitro colonization by Pasteurella haemolytica. Vet Res Commun 22(3):147–153CrossRefGoogle Scholar
  12. Firdaus-Nawi M, Sabri MY, Hanan Y, Siti-Zahrah A, Zamri-Saad M (2014) Efficacy of feed-based adjuvant vaccine against Streptococcus agalactiae in Oreochromis spp. in Malaysia. Aquac Res 45(1):87–96CrossRefGoogle Scholar
  13. Gudding R, Lillehaug A, Evensen Ø (1999) Recent developments in fish vaccinology. Vet Immunol Immunopathol 72(1):203–212CrossRefGoogle Scholar
  14. Hart S, Wrathmell AB, Harris JE, Grayson TH (1988) Gut immunology in fish: a review. Dev Comp Immunol 12(3):453–480CrossRefGoogle Scholar
  15. Iida T, Wakabayashi H, Egusa S (1982) Vaccination for control of streptococcal disease in cultured yellowtail. Fish Pathol 16:201–206CrossRefGoogle Scholar
  16. Irie T, Watarai S, Iwasaki T, Kodoma H (2005) Protection against experimental Aeromonas salmonicida infection in carp by oral immunisation with bacterial antigen entrapped liposomes. Fish Shellfish Immunol 18:235–242CrossRefGoogle Scholar
  17. Isiaku AS, Sabri MY, Ina-Salwany MY, Hassan MD, Tanko PN, Bello MB (2017) Biofilm is associated with chronic streptococcal meningoencephalitis in fish. Microb Pathog 102:59–68CrossRefGoogle Scholar
  18. Jenkins PG, Wrathmell AB, Harris JE, Pulsfored AL (1994) The effects of different adjuvants on intestinal antigen absorption and subsequent immune responses of the tilapia Oreochromis mossambicus. Fish Shellfish Immunol 4:167–177CrossRefGoogle Scholar
  19. Johnson K, Amend D (1983) Efficacy of Vibrio anguillarum and Yersinia ruckeri bacterins applied by oral and anal intubation of salmonids. J Fish Dis 6(5):473–476CrossRefGoogle Scholar
  20. Joosten PHM, Aviles-Trigueros M, Sorgeloos P, Rombout JHWM (1995) Oral vaccine of juvenile carp (Cyprinus carpio) and gilthead seabream (Sparus aurata) with bioencapsulated Vibrio anguillarum bacterin. Fish Shellfish Immunol 5:289–299CrossRefGoogle Scholar
  21. Kiyono H, Bienenstock J, McGhee JR, Ernst PB (1992) The mucosal immune system: features of inductive and effector sites to consider in mucosal immunization and vaccine development. Reg Immunol 4:54–62Google Scholar
  22. Klesius PH, Shoemaker CA, Evans JJ (2000) Efficacy of single and combined Streptococcus iniae isolate vaccine administered by intraperitoneal and intramuscular routes in tilapia (Oreochromis niloticus). Aquaculture 188(3):237–246CrossRefGoogle Scholar
  23. Klesius PH, Evans JJ, Shoemaker CA, Lim C (2006) A US perspective on selected biotechnological advancements in fish health. Aquac Health Int 5:10–12Google Scholar
  24. Liaghat M, Akhlaghi M, Hosseini A, Nematollahi A, Hosseini SM (2011) Humoral and non-specific immune responses in rainbow trout (Oncorhynchus mykiss) naturally exposed to and immunized with Streptococcus iniae. Int J Vet Res 5(4):218–224Google Scholar
  25. Mah T-FC, O’Toole GA (2001) Mechanism of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39CrossRefGoogle Scholar
  26. Moore JD, Ototake M, Nakanishi T (1998) Particulate antigen uptake during immersion immunisation of fish: the effectiveness of prolonged exposure and the roles of skin and gill. Fish Shellfish Immunol 8(6):393–407CrossRefGoogle Scholar
  27. Nayak DK, Asha A, Shankar KM, Mohan C (2004) Evaluation of biofilm of Aeromonas hydrophila for oral vaccination of Clarias batrachus-a carnivore model. Fish Shellfish Immunol 16(5):613–619CrossRefGoogle Scholar
  28. Noraini O, Sabri MY, Siti-Zahrah A (2013) Efficacy of spray administration of formalin-killed Streptococcus agalactiae in hybrid red tilapia. J Aquat Anim Health 25(2):142–148Google Scholar
  29. Nur-Nazifah M, Sabri MY, Siti-Zahrah A (2014) Development and efficacy of feed based recombinant vaccine encoding the cell wall surface anchor family protein of Streptococcus agalactiae against streptococcosis in Oreochromis sp. Fish Shellfish Immunol 37(1):193–200Google Scholar
  30. Piganelli JD, Zhang JA, Christensen JM, Kaattari SL (1994) Enteric coated microspheres as an oral method for antigen delivery to salmonids. Fish Shellfish Immunol 4(3):179–188CrossRefGoogle Scholar
  31. Plumb JA, Hanson LA (2011) Health maintenance and principal microbial diseases of cultured fishes. John Wiley & SonsGoogle Scholar
  32. Quentel C, Vigneulle M (1997) Antigen uptake and immune responses after oral vaccination. Dev Biol Stand 90:69–78Google Scholar
  33. Rombout JHWM, Lamers CHJ, Helfrich MH, Dekker A, Taverne-Thiele JJ (1985) Uptake and transport of intact macromolecules in the intestinal epithelium of carp (Cyprinus carpio L.) and the possible immunological implications. Cell Tissue Res 239(3):519–530CrossRefGoogle Scholar
  34. Siriyappagouder P, Shankar KM, Naveen Kumar BT, Patil R, Byadgi OV (2014) Evaluation of biofilm of Aeromonas hydrophila for oral vaccination of Channa striatus. Fish Shellfish Immunol 41(2):581–585CrossRefGoogle Scholar
  35. Siti-Zahrah A, Misri S, Padilah B, Zulkafli R, Kua BC, Azila A R Rimatulhana. 2004. Pre-disposing factors associated with outbreak of streptococcal infection in floating cage-cultured red tilapia in reservoirs. Abstracts of the 7th Asian Fisheries Forum 04, The Triennial Meeting of The Asian Fisheries Society 30th Nov–4th Dec 2004, Penang, Malaysia. pp. 129.Google Scholar
  36. Soltani M, Jamshidi S, Sharifpour I (2005) Streptococcosis caused by Streptococcus iniae in farmed rainbow trout (Oncorhynchus mykiss) in Iran: biophysical characteristics and pathogenesis. Bull Eur Assoc Fish Pathol 25(3):95–106Google Scholar
  37. Tafalla C, Bogwald J, Dalmo RA (2013) Adjuvants and immunostimulants in fish vaccines: current knowledge and future perspectives. Fish Shellfish Immunol 35(6):1740–1750CrossRefGoogle Scholar
  38. Vandenberg GW (2004) Oral vaccines for finfish: academic theory or commercial reality? Anim Health Res Rev 5(2):301–304CrossRefGoogle Scholar
  39. Wong G, Kaattari LS, Christensen MJ (1992) Effectiveness of an oral enteric coated Vibrio vaccine for use in salmonid fish. Immunol Investig 21:353–364CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • M. Kahieshesfandiari
    • 1
  • M. Y. Sabri
    • 2
    Email author
  • M. Y. Ina-salwany
    • 1
  • M. D. Hassan
    • 3
  • O. Noraini
    • 2
  • A. A. Ajadi
    • 2
  • A. I. Isiaku
    • 2
  1. 1.Department of Aquaculture, Faculty of AgricultureUniversiti Putra MalaysiaSerdangMalaysia
  2. 2.Deparment of Veterinary Pathology & Microbiology, Faculty of Veterinary MedicineUniversiti Putra MalaysiaSerdangMalaysia
  3. 3.Department of Veterinary Clinical, Faculty of Veterinary MedicineUniversiti Putra MalaysiaSerdangMalaysia

Personalised recommendations