Effects of dietary supplementation of citrus by-products fermented with a probiotic microbe on growth performance, innate immunity and disease resistance against Edwardsiella tarda in juvenile olive flounder, Paralichthys olivaceus (Temminck & Schlegel)

Journal of Fish Diseases

Volumn 36, Issue 7, 2013, Pages 617-628

  Lee, B J ^a,c   Kim, S S ^a   Song, J W ^a   Oh, D H ^a   Cha, J H ^a   Jeong, J B ^a   Heo, M S ^a   Kim, K W ^b   Lee, K J ^a  

^a Jeju National University   (South Korea)

^b National Fisheries Research and Development Institute (NFRDI)   (South Korea)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Bacillus subtilis; Citrus by product; Fermentation; Olive flounder; Probiotic bacteria

Indexed keywords

PROBIOTIC AGENT;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; BACILLUS SUBTILIS; CITRUS; DIET; DIET SUPPLEMENTATION; DISEASE RESISTANCE; DOSE RESPONSE; EDWARDSIELLA TARDA; ENTEROBACTERIACEAE INFECTION; ENTEROCOCCUS FAECIUM; FERMENTATION; FISH DISEASE; FLOUNDER; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; INTRAPERITONEAL DRUG ADMINISTRATION; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; MORTALITY;

ANIMAL FEED; ANIMALS; BACILLUS SUBTILIS; CITRUS; DIET; DIETARY SUPPLEMENTS; DISEASE RESISTANCE; DOSE-RESPONSE RELATIONSHIP, DRUG; EDWARDSIELLA TARDA; ENTEROBACTERIACEAE INFECTIONS; ENTEROCOCCUS FAECIUM; FERMENTATION; FISH DISEASES; FLOUNDER; IMMUNITY, INNATE; INJECTIONS, INTRAPERITONEAL; LACTOBACILLUS; PROBIOTICS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); CITRUS; EDWARDSIELLA TARDA; ENTEROCOCCUS FAECIUM; LACTOBACILLUS RHAMNOSUS; PARALICHTHYS OLIVACEUS; PLEURONECTOIDEI;

EID: 84879317714     PISSN: 01407775     EISSN: 13652761     Source Type: Journal    
DOI: 10.1111/jfd.12035     Document Type: Article

References (73)

1. Abee T. & Wouters J.A. (1999) Microbial stress response in minimal processing. International Journal of Food Microbiology 50, 65-91.
2. Ai Q.H., Mai K.S., Zhang C.X., Xu W., Duan Q.Y., Tan B.P. & Liufu Z.G. (2004) Effects of dietary vitamin C on growth and immune response of Japanese seabass, Lateolabrax japonicus. Aquaculture 242, 489-500.
3. Aly S.M., Ahmed Y.A.G., Ghareeb A.A.A. & Mohamed M.F. (2008) Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish and Shellfish Immunology 25, 128-136.
4. Anagnostopoulou M.A., Kefalas P., Papageorgiou V.P., Assimopoulou A.N. & Boskou D. (2006) Radical scavenging activity of various extracts and fractions of sweet orange peel (Citrus sinensis). Food Chemistry 94, 19-25.
5. Anbarasu K. & Chandran M.R. (2001) Effects of ascorbic acid on the immune response of the catfish, Mystus gulio (Hamilton), to different bacterins of Ameromonas hydrophila. Fish and Shellfish Immunology 11, 347-355.
6. AOAC. (1995) Official Methods of Analysis, 16th edn. Association of Official Analytical Chemists, Arlington, VA.
7. Aregheore E.M. (2000) Chemical composition and nutritive value of some tropical by-product feedstuffs for small ruminants in vivo and in vitro digestibility. Animal Feed Science Technology 85, 99-109.
8. Azad I.S., Dayal J.S., Poornima M. & Ali S.A. (2007) Supra dietary levels of vitamins C and E enhance antibody production and immune memory in juvenile milkfish, Chanos chanos to formalin-killed Vibrio vulnificus. Fish and Shellfish Immunology 23, 154-163.
9. Bell G.R., Higgs D.A. & Traxler G.S. (1984) The effect of dietary ascorbate, zinc, and manganese on the development of experimentally induced bacterial kidney disease in sockeye salmon (Oncorhynchus nerka). Aquaculture 36, 293-311.
10. Benavente-García O., Castillo J., Alcaraz M., Vicente V., Del Rio J.A. & Ortuño A. (2007) Beneficial action of citrus flavonoids on multiple cancer related biological pathway. Current Cancer Drug Targets 7, 795-809.
11. Brown B.A. (1980) Routine hematology procedures. In: Hematology, Principles and Procedures (ed. by B.A. Brown ), pp. 71-112. Lea & Febiger, Philadelphia.
12. Cano A., Medinaan A. & Bermejo A. (2008) Bioactive compounds in different citrus varieties. Discrimination among cultivars. Journal of Food Composition and Analysis 21, 377-381.
13. Chandler S.F. & Dodds J.H. (1983) The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanumlaciniatum. Plant Cell Reports 2, 205-208.
14. Chelossi E., Vezzulli L., Milano A., Branzoni M., Fabiano M., Riccardi G. & Banat I.M. (2003) Antibiotic resistance of benthic bacteria in fish-farm and control sediments of the Western Mediterranean. Aquaculture 219, 83-97.
15. Chevassus B. & Dorson M. (1990) Genetics of resistance to diseases in fish. Aquaculture 85, 83-107.
16. Dabrowski K. & Hinterleitner S. (1989) Simultaneous analysis of ascorbic acid, dehydroascorbic acid, and ascorbic sulfate in biological material. Analyst 114, 83-87.
17. Dalmo R.A., Ingebrigtsen K. & Bogwald J. (1997) Non-specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES). Journal of Fish Diseases 20, 241-273.
18. Eo J. & Lee K.J. (2008) Effect of dietary ascorbic acid on growth and non-specific immune responses of tiger puffer, Takifugu rubripes. Fish and Shellfish Immunology 25, 611-616.
19. Fickers P., Guez J.S., Damblon C., Leclere V., Bechet M., Jacques P. & Joris B. (2009) High-level biosynthesis of the anteiso-C (17) isoform of the antibiotic mycosubtilin in Bacillus subtilis and characterization of its candidacidal activity. Applied and Environmental microbiology 75, 4636-4640.
20. Francis G., Makkar P.S. & Becker K. (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197-227.
21. Gatesoupe F.J. (1999) The use of probiotics in aquaculture. Aquaculture 180, 147-165.
22. Gatlin D.M., Barrows F.T., Brown P., Dabrowski K., Gaylord T.G., Hardy R.W., Herman E., Hu G., Krogdahl Å., Nelson R., Overturf K., Rust M., Sealey W., Skonberg D., Souza E.J., Stone D., Wilson R. & Wurtele E. (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquaculture Research 38, 551-579.
23. Grasser K.D. (1995) Plant chromosomal high mobility group (HMG) proteins. The Plant Journal 7, 185-192.
24. Han H.J., Kim D.H., Lee D.C., Kim S.M. & Park S.I. (2006) Pathogenicity of Edwardsiella tarda to olive flounder, Paralichthys olivaceus (Temmick & Schlegel). Journal of Fish Diseases 29, 601-609.
25. Hatamipour M.S., Majidi S.M., Abdi M. & Farbodnia M.A. (2004) Potentials for industrial utilization of citrus by-products. 16th International Congress of Chemical and Process Engineering - Chisa 2004. Czech Society of Chemical Engineering. Prague, Czech Republic, pp. 7-133
26. Inaoka T., Takahashi K., Ohnishi-Kameyama M., Yoshida M. & Ochi K. (2003) Guanine nucleotide guanosine 5′-diphosphate 3′-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. The Journal of Biological Chemistry 278, 2169-2176.
27. Iwata N., Kikuchi K. & Kurokura H. (1995) Growth of brown flounder Paralichthys olivaceus at different temperature. The Israeli Journal of Aquaculture 47, 178-184.
28. Kang H.J., Chawla S.P., Jo C., Kwon J.H. & Byun M.W. (2006) Studies on the development of functional powder from citrus peel. Bioresource Technology 97, 614-620.
29. Kesarcodi-Watson A., Kaspar H., Josie Lategan M. & Gibson L. (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274, 1-8.
30. Kim D.H. & Austin B. (2006) Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish and Shellfish Immunology 21, 513-524.
31. Kino K., Kotanaka Y., Arai T. & Yagasaki M. (2009) A novel L-amino acid ligase from Bacillus subtilis NBRC3134, a microorganism producing peptide-antibiotic rhizoctin. Bioscience, Biotechnology, and Biochemistry 73, 901-907.
32. Kumar R., Mukherjee S.C., Ranjan R. & Nayak S.K. (2008) Enhanced innate immune parameters in Labeo rohita (Ham.) following oral administration of Bacillus subtilis. Fish and Shellfish Immunology 24, 168-172.
33. Kumari J. & Sahoo P.K. (2005) Effects of cyclophosphamide on the immune system and disease resistance of Asian catfish Clarias batrachus. Fish and Shellfish Immunology 19, 307-316.
34. Kwon S.R., Lee E.H., Nam Y.K., Kim S.K. & Kim K.H. (2007) Efficacy of oral immunization with Edwardsiella tarda ghosts against edwardsiellosis in olive flounder (Paralichthys olivaceus). Aquaculture 269, 84-88.
35. Lauzon H.L., Gudmundsdottir S., Pedersen M.H., Budde B.B. & Gudmondsottir B.K. (2008) Isolation of putative probionts from cod rearing environment. Veterinary Microbiology 132, 328-339.
36. Lee S.M., Lee J.H. & Kim K.D. (2003) Effect of dietary essential fatty acids on growth, body composition and blood chemistry of juvenile starry flounder (Platichthys stellatus). Aquaculture 225, 269-281.
37. Li Y. & Lovell R.T. (1985) Elevated levels of dietary ascorbic acid increase immune responses in channel catfish. Journal of Nutrition 115, 123-131.
38. Li S., Lo C.Y. & Ho C.T. (2006) Hydroxylated polymethoxyflavones and methylated flavonoids in sweet orange (Citrus sinensis) peel. Journal of Agricultural and Food Chemistry 54, 4176-4185.
39. Li J., Tan B. & Mai K. (2009) Dietary probiotic Bacillus OJ and isomaltooligosaccharides influence the intestine microbial populations, immune responses and resistance to white spot syndrome virus in shrimp (Litopenaeus vannamei). Aquaculture 291, 35-40.
40. Lim S.J. & Lee K.J. (2009) Partial replacement of fish meal by cottonseed meal and soybean meal with iron and phytase supplementation for parrot fish, Oplegnathus fasciatus. Aquaculture 290, 283-289.
41. Lin M.F. & Shiau S.Y. (2005) Dietary L-ascorbic acid affects growth, nonspecific immune response and disease resistance in juvenile grouper, Epinephelus malabaricus. Aquaculture 244, 215-221.
42. Ma Y., Ye X., Hao Y., Xu G., Xu G. & Liu D. (2008) Ultrasound-assisted extraction of hesperidin from Penggan (Citrus reticulate) peel. Ultrasonics Sonochemistry 15, 227-232.
43. Macey B.M. & Coyne V.E. (2005) Improved growth rate and disease resistance in farmed Haliotis midae through probiotic treatment. Aquaculture 245, 249-261.
44. Magnadottir B. (2006) Innate immunity of fish (overview). Fish and Shellfish Immunology 20, 137-151.
45. 1, 2, 3. The American Journal of Clinical Nutrition 81, 230-242.
46. Middleton E., Kandaswami C. & Theoharides T. (2000) The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacological Reviews 52, 673-751.
47. Ministry of Maritime Affairs & Fisheries. (2009) Aquaculture Statistic from Ministry of Maritime Affairs and Fisheries. Ministry of Maritime Affairs and Fisheries, Seoul, South Korea.
48. Moon Y.G., Lee K.J., Kim K.Y., Song C.B., Jeon Y.J. & Heo M.S. (2006) Characteristics of citrus by-product ferment using probiotics as starter. Korean Journal of Microbiology and Biotechnology 34, 158-165.
49. Navarre O. & Halver J.E. (1989) Disease resistance and humoral antibody production in rainbow trout fed high levels of vitamin C. Aquaculture 79, 207-221.
50. Naviner M., Giraud E., Thorin C., Le Bris H., Pouliquen H. & Ganiere J.P. (2007) Effects of three dosages of oral oxolinic acid treatment on the selection of antibiotic-resistant Aeromonas: experimental approach in farmed trout. Aquaculture 269, 31-40.
51. Nayak S.K., Swain P. & Mukherjee S.C. (2007) Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (Ham). Fish and Shellfish Immunology 23, 892-896.
52. Nogueira-Lima A.C., Gesteira T.C.V. & Mafezoli J. (2006) Oxytetracycline residues in cultivated marine shrimp (Litopenaeus vannamei Boone, 1931) (Crustacea, Decapoda) submitted to antibiotic treatment. Aquaculture 254, 748-757.
53. Ortuño J., Esteban M.A. & Meseguer J. (2003) The effect of dietary intake of vitamins C and E on the stress response of gilthead seabream (Sparus aurata L.). Fish and Shellfish Immunology 14, 145-156.
54. Panigrahi A., Kiron V., Satoh S., Hironol I., Kobayashi T., Sugita H., Puangkaew J. & Aoki T. (2007) Immune modulation and expression of cytokine genes in rainbow trout Oncorhynchus mykiss upon probiotic feeding. Developmental and Comparative Immunology 31, 372-382.
55. Picchietti S., Fausto A.M., Randelli E., Carnevali O., Taddei A.R., Buonocore F., Scapigliati G. & Abelli L. (2009) Early treatment with Lactobacillus delbrueckii strain induces an increase in intestinal T-cell and granulocytes and modulates immune-related genes of larval Dicentrarchus labrax (L.). Fish and Shellfish Immunology 26, 268-376.
56. Qi Z., Zhang X.H., Boon N. & Bossier P. (2009) Probiotics in aquaculture of China - Current state, problems and prospect. Aquaculture 290, 15-21.
57. Roberts M.L., Davies S.J. & Pulsford A.L. (1995) The influence of ascorbic acid (vitamin C) on non-specific immunity in the turbot (Scophthalmus maximus L.). Fish and Shellfish Immunology 5, 27-38.
58. Salinas I., Cuesta A., Esteban M.A. & Meseguer J. (2005) Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combined, on gilthead seabream cellular innate immune responses. Fish and Shellfish Immunology 19, 67-77.
59. Scerra V., Caridi A., Foti F. & Sinatra M.C. (1999) Influence of dairy Penicillium sp. on nutrient content of citrus fruit peel. Animal Feed Science Technology 78, 169-176.
60. Schallmey M., Singh A. & Ward O.P. (2004) Developments in the use of Bacillus species in industrial production. Canadian Journal of Microbiology 50, 1-17.
61. Sendra E., Fayos P., Lario Y., Fernández-López J., Sayas-Barberá E. & Pérez-Alvarez J.A. (2008) Incorporation of citrus fibers in fermented milk containing probiotic bacteria. Food Microbiology 25, 13-21.
62. Shetty K., Curtis O.F., Leven R.E., Witkowsky R. & Ang V. (1995) Prevention of vitrification associated with the in vitro shoot culture of oregano (Origanumvulgare) by Pseudomonas spp. Journal of Physiology 147, 447-451.
63. Song Y.B., Moon S.W., Kim S.J. & Lee Y.D. (2002) Effect of EM-fermented orange in commercial diet on growth of juvenile flounder, Paralichthys olivaceus. Journal of Aquaculture 15, 103-110.
64. Stein T., Borchert S., Kiesau P., Heinzmann S., Kloss S., Klein C., Helfrich M. & Entian K.D. (2002) Dual control of subtilin biosynthesis and immunity in Bacillus subtilis. Molecular Microbiology 44, 403-416.
65. Subasinghe R.P. (2005) Epidemiological approaches to aquatic animal health management: opportunities and challenges for developing countries to increase aquatic production through aquaculture. Preventive Veterinary Medicine 67, 117-124.
66. Taoka Y., Maeda H., Jo J.Y., Jeon M.J., Bai S.C., Lee W.J., Yuge K. & Koshio S. (2006) Growth, stress tolerance and non-specific immune response of Japanese flounder Paralichthys olivaceus to probiotics in a closed recirculation system. Fisheries Science 72, 310-321.
67. Thompson I., White A., Fletcher T.C., Houlihan D.F. & Secombes C.J. (1993) The effect of stress on the immune response of Atlantic salmon (Salmo salar L.) fed diets containing amount of vitamin C. Aquaculture 114, 1-18.
68. Van den Bogaard A.E. & Stobberingh E.E. (2000) Epidemiology of resistance to antibiotic. Links between animals and humans. International Journal of Antimicrobial Agents 14, 327-335.
69. Wang X., Kim K. & Bai S.C. (2002) Effects of different dietary levels of l-ascorbyl-2-polyphosphate on growth and tissue vitamin C concentrations in juvenile olive flounder, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture Research 33, 261-267.
70. Yano T. (1992) Assays of hemolytic complement activity. In: Techniques in Fish Immunology (ed. by J.S. Stolen, T.C. Fletcher, D.P. Anderson, S.L. Kaattari & A.F. Rowley ), pp. 131-141. SOS Publications, Fair Haven.
71. Zhou J., Song X.L., Huang J. & Wang X.H. (2006) Effects of dietary supplementation of A3α-peptidoglycan on innate immune responses and defense activity of Japanese flounder (Paralichthys olivaceus). Aquaculture 251, 172-181.
72. Ziaei-Nejad S., Rezaei M.H., Takami G.A., Lovett D.L., Mirvaghefi A.R. & Shakouri M. (2006) The effect of Bacillus spp. bacteria used as probiotics on digestive enzyme activity, survival and growth in the Indian white shrimp Fenneropenaeus indicus. Aquaculture 252, 516-524.
73. Zielinsaka-Przyjemska M. & Ignatowicz E. (2008) Citrus fruit flavonoids influence on neutrophil apoptosis and oxidative metabolism. Phytotherapy Research 22, 1557-1562.