واکسن‌ها، ادجوانت‌ها و روش‌های مرسوم استفاده از آن‌ها در ماهیان پرورشی

نوع مقاله : مقاله کامل علمی - پژوهشی

نویسندگان

1 نویسنده مسئول، گروه پژوهشی فرآورده‌های بیولوژیک دامی، سازمان جهاد دانشگاهی تهران، تهران، ایران و گروه تکثیر و پرورش آبزیان، دانشکده شیلات و محیط زیست، دانشگاه علوم کشاورزی و منابع طبیعی گرگان، گرگان، ایران

2 گروه زیست‌شناسی سلولی مولکولی و میکروبیولوژی، دانشکده علوم و فناوری‌های زیستی، دانشگاه اصفهان، اصفهان، ایران.

3 گروه تکثیر و پرورش آبزیان، دانشکده شیلات و محیط زیست، دانشگاه علوم کشاورزی و منابع طبیعی گرگان، گرگان، ایران.

چکیده

ایمن‌سازی ماهی با استفاده از واکسن بیش از 50 سال است که انجام می‌شود و به طور کلی به عنوان یک روش موثر برای پیشگیری از طیف گسترده‌ای از بیماری‌های باکتریایی و ویروسی پذیرفته شده است. واکسیناسیون به پایداری زیست‌محیطی، اجتماعی و اقتصادی در آبزی‌پروری جهانی کمک می‌کند. اکثر واکسن‌های تولیدی واکسن‌های غیرفعال هستند که با استفاده از ادجوانت‌ها فرموله شده و از طریق مسیرهای تزریقی، غوطه‌وری یا خوراکی به ماهی تحویل داده می‌شوند. واکسن‌های زنده کارآمدتر از واکسن‌های غیرفعال هستند، زیرا این واکسن‌ها شرایط عفونت‌های بیماری‌زای طبیعی را تقلید می‌کنند و پاسخ آنتی‌بادی قوی ایجاد می‌کنند. متأسفانه، واکسن‌ها معمولاً به تنهایی قادر به ایجاد محافظت نیستند. به ویژه آن دسته از واکسن‌هایی که بر پایه آنتی‌ژن‌های نوترکیب یا پاتوژن‌های غیرفعال هستند. بنابراین، استفاده از ادجوانت‌ها یا محرک‌های ایمنی اغلب برای افزایش کارایی واکسن ضروری هستند و پتانسیل بیشتری برای تجویز از طریق راه‌های تزریقی، خوراکی یا غوطه‌وری دارند. امروزه واکسن‌های جدید (واکسن‌های مخاطی، توکسوئید) و ادجوانت‌های گیاهی بیش از پیش مورد توجه محققان قرار گرفته‌اند و اثرات قابل توجهی در برابر بیماری‌های عفونی داشته‌اند. فناوری‌های پیشرفته نویدبخش آینده واکسن‌های آبزی‌پروری است و مزایای سلامتی و افزایش پتانسیل اقتصادی را برای تولیدکنندگان فراهم خواهند کرد. با توجه به این‌که واکسن‌ها عملکرد‌های ایمنی و پیشگیری کننده در برابر طیف وسیعی از بیماری‌ها را دارند، در این مقاله به انواع واکسن‌ها و ادجوانت‌های آبزیان و روش‌‌های استفاده از آن‌ها پرداختیم.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

Vaccines, adjuvants and conventional methods of using them in farmed fish

نویسندگان [English]

  • Majid Khanzadeh 1
  • Babak Beikzadeh 2
  • Seyed Hossein Hoseinifar 3
1 . Corresponding Author, Animal Biological Product Research Group, Academic Center for Education, Culture and Research (ACECR), Tehran Organization, Tehran, Iran and Dept. of Aquaculture, Faculty of Fisheries and Environmental Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
2 Dept. of Cell and Molecular Biology & Microbiology, Faculty of Biological Sciences and Technology, University of Isfahan, Isfahan, Iran.
3 Dept. of Aquaculture, Faculty of Fisheries and Environmental Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
چکیده [English]

Fish immunization using vaccines has been practiced for more than 50 years and is generally accepted as an effective method for preventing a wide range of bacterial and viral diseases. Vaccination contributes to environmental, economic and social sustainability in global aquaculture. Most of the manufactured vaccines are inactive vaccines that are formulated using adjuvants and delivered to fish through injection, immersion or oral routes. Live vaccines are more effective than inactivated vaccines because they mimic the conditions of natural pathogen infections and elicit a strong antibody response. Unfortunately, vaccines are usually not able to provide protection on their own. Especially those vaccines that are based on recombinant antigens or inactive pathogens. Therefore, the use of adjuvants or immunostimulants is often necessary to increase vaccine efficacy and have more potential to be administered through injection, oral or immersion routes. Nowadays, new vaccines (mucous and toxoid) and herbal adjuvants have been more and more noticed by researchers and have had significant effects against infectious diseases. Advanced technologies hold promise for the future of aquaculture vaccines, providing health benefits and increased economic potential for producers. Considering that vaccines have protective and preventive functions against a wide range of diseases, in this article we discussed the types of vaccines and aquatic adjuvants and their methods of use.

کلیدواژه‌ها [English]

  • Vaccine
  • vaccination
  • adjuvant
  • aquaculture
1.Adel, M., Gholaghaie, M., Binaii, M., Khanjany, P., & Awad, E. (2016). Effect of dietary Achillea wilhelmsii extract on growth performance, and immune status of common carp (Cyprinus carpio). Res. J. Pharm. Biol. Chem. Sci. 7 (6), 1037-46.
2.Rahman, A. N. A., Khalil, A. A., Abdallah H. M., & ElHady, M. (2018). The effects of the dietary supplementation of Echinacea purpurea extract and/or vitamin C on the intestinal histomorphology, phagocytic activity, and gene expression of the Nile tilapia. Fish Shellfish Immunol. 82, 312-8.
3.Kibenge, M. J. T., Iwamoto, T., Wang, Y., Morton, A., Routledge, R., & Kibenge, F. S. B. (2016). Discovery of variant infectious salmon anaemia virus (ISAV) of European genotype in British Columbia, Canada. Virol J .13, 1-17.
4.Ringø, E. (2020). Probiotics in shellfish aquaculture. Aquac. Fish. 5 (1), 1-27..
5.Romero, J., Feijoó, C. G., & Navarrete, P. (2012). Antibiotics in aquaculture–use, abuse and alternatives. Heal Environ. Aquac. 159, 159-98.
6.Romero, J., Ringø, E., & Merrifield, D. L. (2014). The gut microbiota of fish. Aquac Nutr Gut Heal probiotics prebiotics.
75-100.
7.Banerjee, G., & Ray, A. K. (2017). The advancement of probiotics research and its application in fish farming industries. Res. Vet. Sci. 115, 66-77.
8.Pereira, W. A., Mendonça, C. M. N., Urquiza, A. V., Marteinsson, VÞ., LeBlanc, J. G., Cotter, P.D., et al. (2022). Use of Probiotic Bacteria and Bacteriocins as an Alternative to Antibiotics in Aquaculture. Microorganisms. 10 (9), 1705.
9.Costanzo, V., & Roviello, G. N. (2023). The Potential Role of Vaccines in Preventing Antimicrobial Resistance (AMR): An Update and Future Perspectives. Vaccines. 11 (2), 333.
10.Barnes, A. C., Silayeva, O., Landos, M., Dong, H. T., Lusiastuti, A., Phuoc, L. H., et al. (2022). Autogenous vaccination in aquaculture: A locally enabled solution towards reduction of the global antimicrobial resistance problem. Rev. Aquac. 14 (2), 907-18.
11.Wang, B., Thompson, K. D., Wangkahart, E., Yamkasem, J., Bondad‐Reantaso, M. G., Tattiyapong, P., et al. (2023). Strategies to enhance tilapia immunity to improve their health in aquaculture. Rev. Aquac. 15, 41-56.
12.Czochor, J., & Turchick, A. (2014). Focus: Vaccines. Introduction. Yale J. Biol. Med. 87 (4), 401-2.
13.Ma, J., Bruce, T. J., Jones, E. M., & Cain, K. D. (2019). A review of fish vaccine development strategies: Conventional methods and modern biotechnological approaches. Microorganisms. 7 (11), 569.
14.Mohamed, L. A., & Soliman, W. S. (2013). Development and efficacy of fish vaccine used against some bacterial diseases in farmed Tilapa. Nat. Sci. 11 (6), 120-8.
15.Erfanmanesh, A., Beikzadeh, B., & Khanzadeh, M. (2023). Efficacy of polyvalent vaccine on immune response and disease resistance against streptococcosis/lactococcosis and yersiniosis in rainbow trout (Oncorhynchus mykiss). Vet. Res. Commun. 1-9.
16.Adams, A., Aoki, T., Berthe, C., Grisez, L., & Karunasagar, I. (2008). Recent technological advancements on aquatic animal health and their contributions toward reducing disease risks-a review. Dis Asian Aquac VI Colombo, Sri Lanka Fish Heal Sect Asian Fish Soc. 2012, 71–88.
17.Yanong, R. P. E., & Erlacher-Reid, C. (2012). Biosecurity in aquaculture, part 1: an overview. SRAC Publ. 4707, 522.
18.Snieszko, S., Piotrowska, W., Kocylowski, B., & Marek, K. (1938). Badania bakteriologiczne i serogiczne nad bakteriami posocznicy karpi. Mem l’Institut d’Ichtyobiologie Piscic la Stn Piscic Exp a Mydlniki l’Universite Jagiellonienne a Cracovie. 38.
19.Duff, D. C. B. (1942). The oral immunization of trout against Bacterium salmonicida. J. Immunol. 44 (1), 87-94.
20.Mondal, H., & Thomas, J. (2022). A review on the recent advances and application of vaccines against fish pathogens in aquaculture. Aquac Int.1-30.
21.Kumar, G., Menanteau-Ledouble, S., Saleh, M., & El-Matbouli, M. (2015). Yersinia ruckeri, the causative agent
of enteric redmouth disease in fish. Vet. Res. 46 (1), 1-10.
22.Adams, A. (2019). Progress, challenges and opportunities in fish vaccine development. Fish Shellfish Immunol. 90, 210-4.
23.Gudding, R. (2014). Vaccination as a preventive measure. Fish Vaccin. 12-21.
24.Tlaxca, J. L., Ellis, S., & Remmele, Jr RL. (2015). Live attenuated and inactivated viral vaccine formulation and nasal delivery: Potential and challenges. Adv. Drug Deliv. Rev.93, 56-78.
25.Biering, E., Villoing, S., Sommerset, I., & Christie, K. E. (2005). Update on viral vaccines for fish. Dev. Biol. (Basel). 121, 97-113.
26.Baxter, D. (2007). Active and passive immunity, vaccine types, excipients and licensing. Occup Med. (Chic Ill). 57 (8), 552-6.
27.Di Pasquale, A., Preiss, S., Tavares Da Silva, F., & Garçon, N. (2015). Vaccine adjuvants: from 1920 to 2015 and beyond. Vaccines. 3 (2), 320-43.
28.Dadar, M., Dhama, K., Vakharia, V. N., Hoseinifar, S. H., Karthik, K., Tiwari, R., et al. (2017). Advances in aquaculture vaccines against fish pathogens: global status and current trends. Rev. Fish. Sci Aquac. 25 (3), 184-217.
29.Muktar, Y., Tesfaye, S., & Tesfaye, B. (2016). Present status and future prospects of fish vaccination: a review.
J. Vet. Sci. Technol.
7 (02), 299.
30.Bedekar, M. K., & Kole, S. (2022). Types of Vaccines Used in Aquaculture. In: Fish immune system and vaccines. Springer. p. 45-63.
31.Ma, R., Yang, G., Xu, R., Liu, X., Zhang, Y., Ma, Y., et al. (2019). Pattern analysis of conditional essentiality (PACE)-based heuristic identification of an in vivo colonization determinant as a novel target for the construction of a live attenuated vaccine against Edwardsiella piscicida. Fish Shellfish Immunol. 90, 65-72.
32.Sun, Y., Liu, C., & Sun, L. (2010). Isolation and analysis of the vaccine potential of an attenuated Edwardsiella tarda strain. Vaccine. 28 (38), 6344-50.
33.Shoemaker, C.A., Klesius, P.H., Evans, J. J., & Arias, C. R. (2009). Use of modified live vaccines in aquaculture.
J. World Aquac. Soc.
40(5):573–85.
34.Heppell, J., & Davis, H. L. (2000). Application of DNA vaccine technology to aquaculture. Adv. Drug Deliv. Rev.
43 (1), 29-43.
35.LaPatra, S. E., Corbeil, S., Jones, G. R., Shewmaker, W. D., Lorenzen, N., Anderson, E. D., et al. (2001). Protection of rainbow trout against infectious hematopoietic necrosis virus four days after specific or semi-specific DNA vaccination. Vaccine. 19 (28-29), 4011-9.
36.Kurath, G. (2008). Biotechnology and DNA vaccines for aquatic animals. Rev. Sci. Tech. Int des épizooties. 27 (1), 175.
37.Hølvold, L. B., Myhr, A. I., & Dalmo, R. A. (2014). Strategies and hurdles using DNA vaccines to fish. Vet. Res. 45, 1-11.
38.Purcell, M. K., Nichols, K. M., Winton, J. R., Kurath, G., Thorgaard, G. H., Wheeler, P., et al. (2006). Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Mol. Immunol. 43 (13), 2089-106.
39.Utke, K., Kock, H., Schuetze, H., Bergmann, S. M., Lorenzen, N., Einer-Jensen, K., et al. (2008). Cell-media & ted immune responses in rainbow trout after DNA immunization against the viral hemorrhagic septicemia virus. Dev. Comp Immunol. 32 (3), 239-52.
40.Jixiang, C., Shuang, L., Yun, L., Xianghong, W., Zongjun, D., Dehua, Y., et al. (2002). Purification of an extracellular protease from Vibrio anguillarum and its physicochemical properties. Zhongguo Shui Chan ke xue= J. Fish. Sci. China. 9 (4), 318-22.
41.Denkin, S. M., & Nelson, D. R. (2004). Regulation of Vibrio anguillarum empA metalloprotease expression and its role in virulence. Appl. Environ Microbiol. 70 (7), 4193-204.
42.Nusbaum, K. E., Smith, B. F., DeInnocentes, P., & Bird, R.C. (2002). Protective immunity induced by DNA vaccination of channel catfish with early and late transcripts of the channel catfish herpesvirus (IHV-1). Vet. Immunol. Immunopathol. 84 (3-4), 151-68.
43.Reyes, M., Ramírez, C., Ñancucheo, I., Villegas, R., Schaffeld, G., Kriman, L., et al. (2017). A novel “in-feed” delivery platform applied for oral DNA vaccination against IPNV enables high protection in Atlantic salmon (Salmon salar). Vaccine. 35 (4), 626-32.
44.Hu, F., Li, Y., Wang, Q., Wang, G., Zhu, B., Wang, Y., et al. (2020). Carbon nanotube-based DNA vaccine against koi herpesvirus given by intramuscular injection. Fish Shellfish Immunol. 98, 810-8.
45.Pardi, N., Hogan, M. J., Porter, F. W., & Weissman, D. (2018). mRNA vaccines-a new era in vaccinology. Nat. Rev. Drug Discov. 17 (4), 261-79.
46.Perri, S., Greer, C. E., Thudium, K., Doe, B., Legg, H., Liu, H., et al. (2003). An alphavirus replicon particle chimera derived from venezuelan equine encephalitis and sindbis viruses is a potent gene-based vaccine delivery vector. J. Virol. 77 (19), 10394-403.
47.Polo, J. M., Belli, B. A., Driver, D. A., Frolov, I., Sherrill, S., Hariharan, M. J., et al. (1999). Stable alphavirus packaging cell lines for Sindbis virus-and Semliki Forest virus-derived vectors. Proc. Natl. Acad. Sci. 96 (8), 4598-603.
48.Karlsen, M., Villoing, S., Rimstad, E., & Nylund, A. (2009). Characterization of untranslated regions of the salmonid alphavirus 3 (SAV3) genome and construction of a SAV3 based replicon. Virol. J. 6 (1), 1-6.
49.Wolf, A., Hodneland, K., Frost, P., Hoeijmakers, M., & Rimstad, E. (2014). Salmonid alphavirus-based replicon vaccine against infectious salmon anemia (ISA): impact of immunization route and interactions of the replicon vector. Fish Shellfish Immunol. 36 (2), 383-92.
50.Dhar, A. K., & Allnutt, F. (2011). Challenges and opportunities in developing oral vaccines against viral diseases of fish. J. Mar. Sci. Res. Dev. S. 1.
51.Dhar, A. K., Bowers, R. M., Rowe, C. G., & Allnutt, F. C. T. (2010). Expression of a foreign epitope on infectious pancreatic necrosis virus VP2 capsid protein subviral particle (SVP) and immunogenicity in rainbow trout. Antiviral Res. 85 (3), 525-31.
52.Chien, M. H., Wu, S. Y., & Lin, C. H. (2018). Oral immunization with cell-free self-assembly virus-like particles against orange-spotted grouper nervous necrosis virus in grouper larvae, Epinephelus coioides. Vet. Immunol. Immunopathol. 197, 69-75.
53.Thiéry, R., Cozien, J., Cabon, J., Lamour, F., Baud, M., & Schneemann, A. (2006). Induction of a protective immune response against viral nervous necrosis in the European sea bass Dicentrarchus labrax by using betanodavirus virus-like particles. J. Virol. 80 (20), 10201-7.
54.Olsen, C. M., Pemula, A. K., Braaen, S., Sankaran, K., & Rimstad, E. (2013). Salmonid alphavirus replicon is functional in fish, mammalian and insect cells and in vivo in shrimps (Litopenaeus vannamei). Vaccine. 31 (48), 5672-9.
55.Chen, M., Hu, K. F., Rozell, B., Orvell, C., Morein, B., & Liljeström, P. (2002). Vaccination with recombinant alphavirus or immune-stimulating complex antigen against respiratory syncytial virus. J. Immunol. 169 (6), 3208-16.
56.Muñoz-Atienza, E., Díaz-Rosales, P., & Tafalla, C. (2021). Systemic and mucosal B and T cell responses upon mucosal vaccination of teleost fish. Front Immunol. 11, 622377.
57.Munang’andu, H. M., Fredriksen, B. N., Mutoloki, S., Brudeseth, B., Kuo, T. Y., Marjara, I. S., et al. (2012). Comparison of vaccine efficacy for different antigen delivery systems for infectious pancreatic necrosis virus vaccines in Atlantic salmon (Salmo salar L.) in a cohabitation challenge model. Vaccine. 30 (27), 4007-16.
58.Noonan, B., Enzmann, P. J., & Trust, T. J. (1995). Recombinant infectious hematopoietic necrosis virus and viral hemorrhagic septicemia virus glycoprotein epitopes expressed in Aeromonas salmonicida induce protective immunity in rainbow trout (Oncorhynchus mykiss). Appl. Environ. Microbiol. 61 (10), 3586-91.
59.Lecocq-Xhonneux, F., Thiry, M., Dheur, I., Rossius, M., Vanderheijden, N., Martial, J., et al. (1994). A recombinant viral haemorrhagic septicaemia virus glycoprotein expressed in insect cells induces protective immunity in rainbow trout. J. Gen. Virol. 75 (7), 1579-87.
60.Acosta, F., Collet, B., Lorenzen, N., & Ellis, A. E. (2006). Expression of the glycoprotein of viral haemorrhagic septicaemia virus (VHSV) on the surface of the fish cell line RTG-P1 induces type 1 interferon expression in neighbouring cells. Fish Shellfish Immunol. 21 (3), 272-8.
61.Vakharia, V. N. (2005). Sub-unit vaccine for infectious pancreatic necrosis virus. Google Patents.
62.Estepa, A., Thiry, M., & Coll, J. M. (1994). Recombinant protein fragments from haemorrhagic septicaemia rhabdovirus stimulate trout leukocyte anamnestic responses in vitro. J. Gen. Virol. 75 (6), 1329-38.
63.Rao, B. M., Kole, S., Gireesh-Babu, P., Sharma, R., Tripathi, G., & Bedekar, M. K. (2019). Evaluation of persistence, bio-distribution and environmental transmission of chitosan/PLGA/pDNA vaccine complex against Edwardsiella tarda in Labeo rohita. Aquaculture. 500, 385-92.
64.Mohamad, A., Zamri-Saad, M., Amal, M. N. A., Al-Saari, N., Monir, M. S., Chin, Y. K., et al. (2021). Vaccine efficacy of a newly developed feed-based whole-cell polyvalent vaccine against vibriosis, streptococcosis and motile aeromonad septicemia in Asian Seabass, Lates calcarifer. Vaccines. 9 (4), 368.
65.Busch, R. A. (1997). Polyvalent vaccines in fish: the interactive effects of multiple antigens. Dev. Biol. Stand. 90, 245-56.
66.Ma, Y., Zhang, Y., & Zhao, D. (2010). Polyvalent attenuated live vaccine for preventing and curing vibriosis of cultivated fish. Google Patents.
67.Brudeseth, B. E., Wiulsrød, R., Fredriksen, B. N., Lindmo, K., Løkling, K. E., Bordevik, M., et al. (2013). Status and future perspectives of vaccines for industrialised fin-fish farming. Fish Shellfish Immunol. 35 (6), 1759-68.
68.Abu-Elala, N. M., Samir, A., Wasfy, M., & Elsayed, M. (2019). Efficacy of injectable and immersion polyvalent vaccine against streptococcal infections in broodstock and offspring of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 88, 293-300.
69.Angelidis, P., Karagiannis, D., & Crump, E. M. (2006). Efficacy of a Listonella anguillarum (syn. Vibrio anguillarum) vaccine for juvenile sea bass Dicentrarchus labrax. Dis. Aquat. Organ. 71 (1), 19-24.
70.Mikkelsen, H., Lund, V., Larsen, R., & Seppola, M. (2011). Vibriosis vaccines based on various sero-subgroups of Vibrio anguillarum O2 induce specific protection in Atlantic cod (Gadus morhua L.) juveniles. Fish Shellfish Immunol. 30 (1), 330-9.
71.Galindo-Villegas, J., Mulero, I., García-Alcazar, A., Muñoz, I., Peñalver-Mellado, M., Streitenberger, S., et al. (2013). Recombinant TNFα as oral vaccine adjuvant protects European sea bass against vibriosis: insights into the role of the CCL25/CCR9 axis. Fish Shellfish Immunol. 35 (4), 1260-71.
72.Siwicki, A. K., Morand, M., Terech‐Majewska, E., Niemczuk, W., Kazuń, K., & Glabski, E. (1998). Influence of immunostimulants on the effectiveness of vaccines in fish: in vitro and in vivo study. J. Appl. Ichthyol. 14 (3‐4), 225-7.
73.Raida, M. K., Nylén, J., Holten-Andersen, L., & Buchmann, K. (2011). Association between plasma antibody response and protection in rainbow trout Oncorhynchus mykiss immersion vaccinated against Yersinia ruckeri. PLoS One. 6 (6), e18832.
74.Skov, J., Kania, P. W., Holten-Andersen, L., Fouz, B., & Buchmann, K. (2012). Immunomodulatory effects of dietary β-1, 3-glucan from Euglena gracilis in rainbow trout (Oncorhynchus mykiss) immersion vaccinated against Yersinia ruckeri. Fish Shellfish Immunol. 33 (1), 111-20.
75.Ghosh, B., Nguyen, T. D., Crosbie, P. B. B., Nowak, B. F., & Bridle, A. R. (2016). Oral vaccination of first-feeding Atlantic salmon, Salmo salar L., confers greater protection against yersiniosis than immersion vaccination. Vaccine.
34 (5), 599-608.
76.Jaafar, R. M., Al‐Jubury, A., Chettri, J. K., Dalsgaard, I., Kania, P. W., & Buchmann, K. (2018). Secondary immune response of rainbow trout following repeated immersion vaccination. J. Fish. Dis. 41 (1), 117-23.
77.Erfanmanesh, A., Mohajerfar, T., Nikaein, D., Mokhtari, A., & Beikzadeh, B. (2022). Comparative protection of two antigens (whole-cell and outer membrane vesicle) of Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Iran J. Fish Sci. 21 (1), 187-201.
78.Mazandarani, M., Hoseinifar, S. H., Reza Gholi Tabar, Z., Sudagar, M., & Safari, R. (2022). Evaluation of Yersinia ruckeri vaccine performance in rainbow trout (Oncorhynchus mykiss). Util Cultiv. Aquat. 11 (2), 37-48.
79.Halimi, M., Alishahi, M., Abbaspour, M. R., Ghorbanpoor, M., & Tabandeh, M. R. (2020). High efficacy and economical procedure of oral vaccination against Lactococcus garvieae/Streptococcus iniae in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 99, 505-13.
80.Soltani, M., Alishahi, M., Mirzargar, S., & Nikbakht, G. (2007). Vaccination of rainbow trout against Streptococcus iniae infection: comparison of different routes of administration and different vaccines. Iran J. Fish. Sci. 7 (1), 129-40.
81.Thinh, N. H., Kuo, T. Y., Hung, L. T., Loc, T. H., Chen, S. C., Evensen, Ø.,
et al. (2009). Combined immersion and oral vaccination of Vietnamese catfish (Pangasianodon hypophthalmus) confers protection against mortality caused by Edwardsiella ictaluri. Fish Shellfish Immunol. 27 (6), 773-6.
82.Du, Y., Tang, X., Sheng, X., Xing, J., & Zhan, W. (2015). Immune response of flounder (Paralichthys olivaceus) was associated with the concentration of inactivated Edwardsiella tarda and immersion time. Vet. Immunol. Immunopathol. 167 (1-2), 44-50.
83.Xiao, J., Chen, T., Liu, B., Yang, W., Wang, Q., Qu, J., et al. (2013). Edwardsiella tarda mutant disrupted in type III secretion system and chorismic acid synthesis and cured of a plasmid as a live attenuated vaccine in turbot. Fish Shellfish Immunol. 35 (3), 632-41.
84.Triet, T. H., Tinh, B. T. T., Hau, L. V., Huong, T. V., & Binh, N. Q. (2019). Development and potential use of an Edwardsiella ictaluri wzz mutant as a live attenuated vaccine against enteric septicemia in Pangasius hypophthalmus (Tra catfish). Fish Shellfish Immunol. 87, 87-95.
85.Gao, Y., Tang, X., Sheng, X., Xing, J., & Zhan, W. (2016). Antigen uptake and expression of antigen presentation-related immune genes in flounder (Paralichthys olivaceus) after vaccination with an inactivated Edwardsiella tarda immersion vaccine, following hyperosmotic treatment. Fish Shellfish Immunol. 55, 274-80.
86.Salonius, K., Siderakis, C., MacKinnon, A. M., & Griffiths, S. G. (2005). As a live vaccine against. Dev. Biol. Basel. 121, 189-97.
87.Ravid-Peretz, S., Colorni, A., Sharon, G., & Ucko, M. (2019). Vaccination of European sea bass Dicentrarchus labrax with avirulent Mycobacterium marinum (iipA:: kan mutant). Fish Shellfish Immunol. 90, 317-27.
88.Ziklo, N., Colorni, A., Gao, L., Du, S. J., & Ucko, M. (2018). Humoral and Cellular Immune Response of European Seabass Dicentrarchus labrax Vaccinated with Heat‐Killed Mycobacterium marinum (iipA:: kan Mutant). J. Aquat. Anim. Health. 30 (4), 312-24.
89.Bøgwald, J., & Dalmo, R. A. (2019). Review on immersion vaccines for fish: An update 2019. Microorganisms. 7 (12), 627.
90.Costa, A. A., Leef, M. J., Bridle, A. R., Carson, J., & Nowak, B. F. (2011). Effect of vaccination against yersiniosis on the relative percent survival, bactericidal and lysozyme response of Atlantic salmon, Salmo salar. Aquaculture. 315 (3-4), 201-6.
91.Nguyen, T. D., Crosbie, P. B. B., Nowak, B. F., & Bridle, A R. (2018). The effects of inactivation methods of Yersinia ruckeri on the efficacy of single dip vaccination in Atlantic salmon (Salmo salar). J. Fish Dis.41 (7), 1173-6.
92.Thornton, J. C., Garduno, R. A., Newman, S. G., & Kay, W. W. (1991). Surface-disorganized, attenuated mutants of Aeromonas salmonicida as furunculosis live vaccines. Microb. Pathog. 11 (2), 85-99.
93.Shoemaker, C. A., Klesius, P. H., Drennan, J. D., & Evans, J. J. (2011). Efficacy of a modified live Flavobacterium columnare
vaccine in fish. Fish Shellfish Immunol. 30 (1), 304-8.
94.Kitiyodom, S., Kaewmalun, S., Nittayasut, N., Suktham, K., Surassmo, S., Namdee, K., et al. (2019). The potential of mucoadhesive polymer in enhancing efficacy of direct immersion vaccination against Flavobacterium columnare infection in tilapia. Fish Shellfish Immunol. 86, 635-40.
95.Zhang, M., Zhang, T., He, Y., Cui, H., Li, H., Xu, Z., et al. (2023). Immunogenicity and protective efficacy of OmpA subunit vaccine against Aeromonas hydrophila infection in Megalobrama amblycephala: An effective alternative to the inactivated vaccine. Front Immunol. 14, 1133742.
96.Vendramin, N., Alencar, A. L. F., Iburg, T. M., Dahle, M. K., Wessel, Ø., Olsen, A. B., et al. (2018). Piscine orthoreovirus infection in Atlantic salmon (Salmo salar) protects against subsequent challenge with infectious hematopoietic necrosis virus (IHNV). Vet. Res. 49, 1-12.
97.Fernandez-Alonso, M., Rocha, A., & Coll, J. M. (2001). DNA vaccination by immersion and ultrasound to trout
viral haemorrhagic septicaemia virus. Vaccine. 19 (23-24), 3067-75.
98.Lund, M., Røsæg, M. V., Krasnov, A., Timmerhaus, G., Nyman, I. B., Aspehaug, V., et al. (2016). Experimental Piscine orthoreovirus infection mediates protection against pancreas disease in Atlantic salmon (Salmo salar). Vet. Res. 47 (1), 1-16.
99.Caruffo, M., Maturana, C., Kambalapally, S., Larenas, J., & Tobar, J. A. (2016). Protective oral vaccination against infectious salmon anaemia virus in Salmo salar. Fish Shellfish Immunol. 54, 54-9.
100.Zhang, C., Zheng, Y. Y., Gong, Y. M., Zhao, Z., Guo, Z. R., Jia, Y. J., et al. (2019). Evaluation of immune response and protection against spring viremia of carp virus induced by a single-walled carbon nanotubes-based immersion DNA vaccine. Virology. 537, 216-25.
101.Aonullah, A. A., Nuryati, S., & Alimuddin, M. S. (2017). Efficacy of koi herpesvirus DNA vaccine administration by immersion method on Cyprinus carpio field scale culture. Aquac. Res. 48 (6), 2655-62.
102.Mohan, T., Verma, P., & Rao, D. N. (2013). Novel adjuvants & delivery vehicles for vaccines development: a road ahead. Indian J. Med. Res. 138 (5), 779.
103.Raman, R. P., & Kumar, S. (2022). Adjuvants for fish vaccines. In: Fish immune system and vaccines. Springer. p. 231-44.
104.Tafalla, C., Bøgwald, J., & Dalmo, R. A. (2013). Adjuvants and immunostimulants in fish vaccines: current knowledge and future perspectives. Fish Shellfish Immunol. 35 (6), 1740-50.
105.Li, J., Tang, L., Li, S., Li, G., & Mo, Z. (2020). The efficacy and side-effects of oil-based adjuvants emulsified Vibrio anguillarum bivalent inactivated vaccine in turbot (Scophthalmus maximus) under production mode. Aquaculture. 524, 735259.
106.Bøgwald, J., & Dalmo, R. A. (2012). Developments in adjuvants for fish vaccines. In: Infectious Disease in Aquaculture. Elsevier. p. 244-74.
107.Gjessing, M. C., Falk, K., Weli, S. C., Koppang, E. O., & Kvellestad, A. (2012). A sequential study of incomplete Freund’s adjuvant-induced peritonitis in Atlantic cod. Fish Shellfish Immunol. 32 (1), 141-50.
108.Ravelo, C., Magariños, B., Herrero, M. C., Costa, L., Toranzo, A. E., & Romalde, J. L. (2006). Use of adjuvanted vaccines to lengthen the protection against lactococcosis in rainbow trout (Oncorhynchus mykiss). Aquaculture. 251 (2-4), 153-8.
109.Coffman, R. L., Sher, A., & Seder, R. A. (2010). Vaccine adjuvants: putting innate immunity to work. Immunity. 33 (4), 492-503.
110.Mulvey, B., Landolt, M. L., & Busch, R. A. (1995). Effects of potassium aluminium sulphate (alum) used in an Aeromonas salmonicida bacterin on Atlantic salmon, Salmo salar L. J. Fish. Dis. 18 (6), 495-506.
111.Jiao, X., Cheng, S., Hu, Y., & Sun, L. (2010). Comparative study of the effects of aluminum adjuvants and Freund’s incomplete adjuvant on the immune response to an Edwardsiella tarda major antigen. Vaccine. 28 (7), 1832-7.
112.Rørstad, G., Aasjord, P. M., & Robertsen, B. (1993). Adjuvant effect of a yeast glucan in vaccines against furunculosis in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol. 3 (3), 179-90.
113.Ogier de Baulny, M., Quentel, C., Fournier, V., Lamour, F., & Le Gouvello, R. (1996). Effect of long-term oral administration of beta-glucan as an immunostimulant or an adjuvant on some non-specific parameters of the immune response of turbot Scophthalmus maximus. Dis. Aquat. Organ. 26 (2), 139-47.
114.Caipang, C. M. A., Hirono, I., & Aoki, T. (2005). Induction of antiviral state in fish cells by Japanese flounder, Paralichthys olivaceus, interferon regulatory factor-1. Fish Shellfish Immunol. 19 (1), 79-91.
115.Sanchez, E., Coll, J., & Tafalla, C. (2007). Expression of inducible CC chemokines in rainbow trout (Oncorhynchus mykiss) in response to a viral haemorrhagic septicemia virus (VHSV) DNA vaccine and interleukin 8. Dev. Comp. Immunol. 31 (9), 916-26.
116.Hoel, K., & Lillehaug A. (1997). Adjuvant activity of polar glycopeptidolipids fromMycobacterium chelonaein experimental vaccines againstAeromonas salmonicidain salmonid fish. Fish Shellfish Immunol.7 (6), 365-76.
117.Kamilya, D., Maiti, T. K., Joardar, S. N., & Mal, B. C. (2006). Adjuvant effect of mushroom glucan and bovine lactoferrin upon Aeromonas hydrophila vaccination in catla, Catla catla (Hamilton). J. Fish. Dis. 29 (6), 331-7.
118.Marana, M. H., Sepúlveda, D., Chen, D., Al-Jubury, A., Jaafar, R. M., Kania, P. W., et al. (2019). A pentavalent vaccine for rainbow trout in Danish aquaculture. Fish Shellfish Immunol. 88, 344-51.
119.Villumsen, K. R., Koppang, E. O., & Raida, M. K. (2015). Adverse and long-term protective effects following oil-adjuvanted vaccination against Aeromonas salmonicida in rainbow trout. Fish Shellfish Immunol. 42 (1), 193-203.
120.He, L., Wu, L., Tang, Y., Lin, P., Zhai, S., Xiao, Y., et al. (2020). Immunization of a novel outer membrane protein from Aeromonas hydrophila simultaneously resisting A. hydrophila and Edwardsiella anguillarum infection in European eels (Angullia angullia). Fish Shellfish Immunol. 97, 300-12.
121.Ramos-Espinoza, F. C., Cueva-Quiroz, V. A., Yunis-Aguinaga, J., Alvarez-Rubio, N. C., de Mello, N. P., &
de Moraes, J. R. E. (2020). Efficacy of two adjuvants administrated with a novel hydrogen peroxide-inactivated vaccine against Streptococcus agalactiae in Nile tilapia fingerlings. Fish Shellfish Immunol. 105, 350-8.
122.Ellul, R. M., Bulla, J., Brudal, E., Colquhoun, D., Wergeland, H., & Rønneseth, A. (2019). Protection and antibody reactivity in lumpsucker (Cyclopterus lumpus L.) following vaccination against Pasteurella sp. Fish Shellfish Immunol. 95, 650-8.
123.Huang, P., Cai, J., Yu, D., Tang, J., Lu, Y., Wu, Z., et al. (2019). An IL-6 gene in humphead snapper (Lutjanus sanguineus): Identification, expression analysis and its adjuvant effects on Vibrio harveyi OmpW DNA vaccine. Fish Shellfish Immunol. 95, 546-55.
124.Hwang, J. Y., Kwon, M. G., Kim, Y. J., Jung, S. H., Park, M. A., & Son, M. H. (2017). Montanide IMS 1312 VG adjuvant enhances the efficacy of immersion vaccine of inactivated viral hemorrhagic septicemia virus (VHSV) in olive flounder, Paralichthys olivaceus. Fish Shellfish Immunol. 60, 420-5.
125.Xu, W., Jiao, C., Bao, P., Liu, Q., Wang, P., Zhang, R., et al. (2019). Efficacy of MontanideTM ISA 763 A VG as aquatic adjuvant administrated with an inactivated Vibrio harveyi vaccine in turbot (Scophthalmus maximus L.). Fish Shellfish Immunol. 84, 56-61.
126.Soltani, M., Mokhtari, A., Mirzargar, S. S., Taherimirghaed, A., Zargar, A., Shafiei, S., et al. (2016). Efficacy and immune response of intraperitoneal vaccination of rainbow trout (Oncorhynchus mykiss) with a Yersinia ruckeri bacterin formulated with MontanideTM ISA 763 AVG adjuvant. Bull. Eur. Assoc. Fish. Pathol. 36 (6), 225-36.
127.Nguyen, H. T., Nguyen, T. T. T, Tsai, M. A., Ya-Zhen, E., Wang, P. C., & Chen, S. C. (2017). A formalin-inactivated vaccine provides good protection against Vibrio harveyi infection in orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol. 65, 118-26.
128.Kwon, H. C., & Kang, Y. J. (2016). Effects of a subunit vaccine (FlaA) and immunostimulant (CpG-ODN 1668) against Vibrio anguillarum in tilapia (Oreochromis niloticus). Aquaculture. 454, 125-9.
129.Hoare, R., Jung, S. J., Ngo, T. P. H., Bartie, K., Bailey, J., Thompson, K. D., et al. (2019). Efficacy and safety of a non-mineral oil adjuvanted injectable vaccine for the protection of Atlantic salmon (Salmo salar L.) against Flavobacterium psychrophilum. Fish Shellfish Immunol. 85, 44-51.
130.Citarasu, T. (2010). Herbal biomedicines: a new opportunity for aquaculture industry. Aquac Int. 18 (3), 403-14.
131.Van Hai, N. (2015). The use of medicinal plants as immunostimulants in aquaculture: A review. Aquaculture. 446, 88-96.
132.Aly, S. M., Al Zohairy, M. A., Rahmani, A. H., Fathi, M., & Atti, N. M. A. (2016). Trials to improve the response of Orechromis niloticus to Aeromonas hydrophila vaccine using immunostimulants (garlic, Echinacea) and probiotics (Organic GreenTM and Vet-YeastTM). African J. Biotechnol. 15 (21), 989-94.
133.Guz, L., Puk, K., Walczak, N., Oniszczuk, T., & Oniszczuk, A. (2014). Effect of dietary supplementation with Echinacea purpurea on vaccine efficacy against infection with Flavobacterium columnare in zebrafish (Danio rerio). Pol J. Vet. Sci. 17 (4).
134.Zaheri Abdevand, L., Soltani, M., & Shafiei, S. (2021). Adjuvant effect of Licorice (Glycyrrhiza glabra) extract on the efficacy of lactococcosis vaccine in rainbow trout (Oncorhynchus mykiss). Iran J. Fish. Sci. 20 (3), 646-62.
135.Abdy, E., Alishahi, M., Tollabi, M., Ghorbanpour, M., & Mohammadian, T. (2017). Comparative effects of Aloe vera gel and Freund’s adjuvant in vaccination of common carp (Cyprinus carpio L.) against Aeromonas hydrophila. Aquac. Int. 25, 727-42.
136.Dhayanithi, N. B., Kumar, T. T. A., Arockiaraj, J., Balasundaram, C., & Harikrishnan, R. (2015). Dietary supplementation of Avicennia marina extract on immune protection and disease resistance in Amphiprion sebae against Vibrio alginolyticus. Fish Shellfish Immunol. 45 (1), 52-8.
137.Wang, Y., Wang, X., Huang, J., & Li, J. (2016). Adjuvant effect of Quillaja saponaria saponin (QSS) on protective efficacy and IgM generation in turbot (Scophthalmus maximus) upon immersion vaccination. Int. J. Mol. Sci. 17 (3), 325.