Advertisement

Effect of dietary Moringa oleifera leaf on the immune response and control of Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus) fry

  • Eman A. Abd El-Gawad
  • Amel M. El Asely
  • Eman I. Soror
  • Amany A. Abbass
  • Brian AustinEmail author
Article
  • 66 Downloads

Abstract

Natural plant dietary supplementation in aquafeed could be used as an effective way for increasing the immunocompetency and disease resistance of fish. The current study aimed to investigate the potential effects of dietary Moringa oleifera leaf powder supplementation on the immune response, antioxidant status, and disease resistance against Aeromonas hydrophila in Oreochromis niloticus. A total of 180 fish (of 2.6 ± 0.5 g average weight) were randomly divided into three groups and fed on basal diet (= controls), and 1.5 and 5% (w/w) M. oleifera leaf powder incorporated into diets for 60 days. After the feeding trial, fish were challenged with A. hydrophila and continued on the same feeding regime during the next 2 weeks. Oral administration of O. niloticus fry with M. oleifera leaf powder led to significantly enhanced immune responses, i.e., respiratory burst, phagocytic and lysozyme activities, IgM level, and antioxidant enzyme activities, namely superoxide dismutase, catalase, and glutathion peroxidase levels in the liver, kidneys, and spleen. Conversely, the malondialdehyde level decreased significantly in the liver and kidneys. There was a significant increase in white blood cell count and non-significant change in red blood cell count and hemoglobin levels. Following challenge with A. hydrophila, all the fish in the experimental groups survived compared to only 20% of the controls; the relative percent survival was 100%. However, there was not any significant effect on growth as a result of feeding with the experimental diets. These results suggested that M. oleifera leaf powder-supplemented diets could enhance the immune response of O. niloticus fry and prevent disease caused by A. hydrophila.

Keywords

Aeromonas hydrophila Antioxidant enzymes Food supplement Immune response Moringa oleifera Oreochromis niloticus 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable national and institutional (Faculty Ethical Research Committee No BUFVTM 02/08/2018) guidelines for the care and use of animals were followed by the authors.

References

  1. Abdel Gawad EA, AM A EL-l, Shourbela RM (2016) Enhancement of antioxidant activity, Non-specific Immunity and growth performance of Nile tilapia (Oreochromis niloticus) by dietary fructooligosaccharides. J Aquacult Res Devel 7:427Google Scholar
  2. Abreu AC, McBain AJ, Simoes M (2012) Plants as sources of new antimicrobials and resistance-modifying agents. Nat Prod Rep 29:1007–1021PubMedCrossRefGoogle Scholar
  3. Adams SM, Brown AM, Goede RW (1993) A quantitative health assessment index for rapid evaluation of fish condition in the field. Trans Am Fish Soc 122:63–73CrossRefGoogle Scholar
  4. Aebi H (1984) Catalase. In: Bergmeyer HU (ed) Methods in Enzymatic Analysis. Academic Press, New York, pp 276–286Google Scholar
  5. Afuang W, Siddhuraju P, Becker K (2003) Comparative nutritional evaluation of raw, methanol extracted residues and methanol extracts of moringa (Moringa oleifera Lam.) leaves on growth performance and feed utilization in Nile tilapia (Oreochromis niloticus L.). Aquacult Res 34:1147–1159CrossRefGoogle Scholar
  6. Altunoglu YC, Bilen S, Ulu F, Biswas G (2017) Immune responses to methanolic extract of black cumin (Nigella sativa) in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 67:103–109CrossRefGoogle Scholar
  7. Amend DF (1981) Potency testing of fish vaccines. Fish Biologics: Serodiagnostics and Vaccines 49:447–454Google Scholar
  8. Anderson D, Siwicki A (1995) Basic haematology and serology for fish health programs. In: Shariff M, Arthur JR, Subasinghe JP (eds) Diseases in Asian Aquaculture II. Fish Health Section. Asian Fisheries Society, Manila, pp 185–202Google Scholar
  9. Anwar F, Latif S, Ashraf M, Gilani AH (2007) Moringa oleifera: a food plant with multiple medicinal uses. Phytother Res 21:17–25PubMedCrossRefGoogle Scholar
  10. AOAC (1995) Official Methods of Analysis of the Association of Official Analytical Chemistry, sixteenth edn. AOAC International, Washington, p 1141Google Scholar
  11. Atli G, Alptekin O, Tukel S, Canli M (2006) Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol 143:218–224CrossRefGoogle Scholar
  12. Austin B, Austin DA (1989) Method for microbiological examination of fish and shellfish. Ellis Horwood, Chichester, pp 317–327Google Scholar
  13. Awad E, Cerezuela R, Esteban MA (2015) Effects of fenugreek (Trigonella foenumgraecum) on gilthead sea bream (Sparus aurata L.) immune status and growth performance. Fish Shellfish Immunol 45:454–464PubMedCrossRefGoogle Scholar
  14. Blaxhall PC, Daisley KW (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781CrossRefGoogle Scholar
  15. Braun N, De-Lima RL, Baldisserotto B, Dafre AL, De-Oliveira Nuñer AP (2010) Growth, biochemical and physiological responses of Salminus brasiliensis with different stocking densities and handling. Aquaculture 301:22–30CrossRefGoogle Scholar
  16. Büyükdeveci ME, Balcázar JL, Demirkale I, Dikel S (2018) Effects of garlic-supplemented diet on growth performance and intestinal microbiota of rainbow trout (Oncorhynchus mykiss). Aquaculture 486:170–174CrossRefGoogle Scholar
  17. Campbell TW (2004) Hematology of lower vertebrates. In: ACVP and ASVCP (ed) 55th Annual meeting of the American College of Veterinary For. Pathol. (ACVP) and 39th Annual meeting of the American Society of Clinical Pathology (ASVCP). International Veterinary Information Service, Ithaca, pp 1104–1214Google Scholar
  18. Dewangan G, Koley KM, Vadlamudi VP, Mishra A, Poddar A, Hirpurkar SD (2010) Antibacterial activity of Moringa oleifera (drumstick) root bark. J Chem Pharm Res 2:424–428Google Scholar
  19. Dhayanithi NB, Ajithkumar TT, Arockiaraj J, Balasundaram C, Ramasamy H (2015) Immune protection by Rhizophora apiculata in clownfish against Vibrio alginolyticus. Aquaculture 446:1–6CrossRefGoogle Scholar
  20. El Asely AM, Abbass A, Austin B (2014) Honeybee pollen improves growth, immunity and protection of Nile tilapia (Oreochromis niloticus) against infection with Aeromonas hydrophila. Fish Shellfish Immunol. 40:500–506PubMedCrossRefGoogle Scholar
  21. Elabd H, Wang HP, Shaheen A, Yao H, Abbass A (2016) Feeding Glycyrrhiza glabra (liquorice) and Astragalus membranaceus (AM) alters innate immune and physiological responses in yellow perch (Perca flavescens). Fish Shellfish Immunol 54:374–384PubMedCrossRefGoogle Scholar
  22. Elgendy MY, Hakim AS, Ibrahim TB, Soliman WS, Ali SE (2016) Immunomodulatory effects of curcumin on Nile tilapia and its antimicrobial properties against Vibrio alginolyticus. J Fish Aquat Sci 11:206–215CrossRefGoogle Scholar
  23. Fazio F (2019) Fish hematology analysis as an important tool of aquaculture: A review. Aquaculture 500:237–242CrossRefGoogle Scholar
  24. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227CrossRefGoogle Scholar
  25. Gültepe N, Bilen S, Yılmaz S, Güroy D, Aydın S (2014) Effects of herbs and spice on health status of tilapia (Oreochromis mossambicus) challenged with Streptococcus iniae. Acta Vet Brno 83:125–131CrossRefGoogle Scholar
  26. Harikrishnan R, Balasundaram CF, Heo MS (2011) Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish. Aquaculture 317:1–15CrossRefGoogle Scholar
  27. Holt JG, Krieg NR, Sneath PHA (1994) Bergey’s Manual of Determinative Bacteriology, 9th edn. Baltimore, Williams and Wilkins CoGoogle Scholar
  28. Hoseinifar SH, Khodadadian ZH, Kolangi MH, Doan HV, Romano N, Dadar M (2017) Enrichment of common carp (Cyprinus carpio) diet with medlar (Mespilus germanica) leaf extract: effects on skin mucosal immunity and growth performance. Fish Shellfish Immunol 67:346–352PubMedCrossRefGoogle Scholar
  29. Houston AH (1997) Are the classical haematological variables acceptable indicators of fish health? Trans Am Fish Soc 126:879–894CrossRefGoogle Scholar
  30. Immanuel G, Uma RP, Iyapparaj P, Citarasu T, Punitha PSM, Michael BM, Palavesam A (2009) Dietary medicinal plant extracts improve growth, immune activity and survival of tilapia Oreochromis mossambicus. J Fish Biol 74:1462–1475PubMedCrossRefGoogle Scholar
  31. Johnson IT, Gee JM, Price K, Curl C, Fenwick GR (1986) Influence of saponins on gut permeability and active nutrient transport in vitro. J.Nutr 116:2270–2277PubMedCrossRefPubMedCentralGoogle Scholar
  32. Karunasagar I, Karunasagar I, Otta SK (2003) Disease problems affecting fish in tropical environments. J Appl Aquacult 13:231–249CrossRefGoogle Scholar
  33. Kazeem GO, Adedayo FE, Thomas AO (2017) Effects of dietary Moringa oleifera extract against Aeromonas hydrophila infection and transportation-induced stress in African catfish Clarias gariepinus (Burchell, 1822) fingerlings. Wld Appl Sci J 35:88–95Google Scholar
  34. Khalil F, Korni FMM (2017) Evaluation of Moringa oleifera leaves and their aqueous extract in improving growth, immunity and mitigating effect of stress on common carp (Cyprinus carpio) fingerlings. Turkish J Aquat Sci 32:170177 CrossRefGoogle Scholar
  35. Kucukbay FZ, Yazlak H, Karaca I, Sahin N, Tuzcu M, Cakmak MN, Sahin K (2009) The effects of dietary organic or inorganic selenium in rainbow trout (Oncorhynchus mykiss) under crowding conditions. Aquacult Nutr 15:569–576CrossRefGoogle Scholar
  36. Lee RG, Foerster J, Jukens J, Paraskevas F, Greer JP, Rodgers GM (1998) Wintrobe’s-Clinical Hematology, 10th edn. Lippincott Williams & Wilkins, New YorkGoogle Scholar
  37. Leone A, Spada A, Battezzati A, Schiraldi A, Aristil J, Bertoli S (2015) Cultivation, genetic, ethnopharmacology, phytochemistry and pharmacology of Moringa oleifera leaves: An overview. Int J Mol Sci 16:12791–12835PubMedPubMedCentralCrossRefGoogle Scholar
  38. Lim SJ, Jang E, Lee SH, Yoo BH, Kim SK, Kim TH (2013) Antibiotic resistance in bacteria isolated from freshwater aquacultures and prediction of the persistence and toxicity of antimicrobials in the aquatic environment. J Environ Sci Hlth B 48:495–504CrossRefGoogle Scholar
  39. Livingstone D (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Méd Vét 154:427–430Google Scholar
  40. Musthafa MS, Asgaria SM, Kurianc A, Elumalaic P, Ali ARJ, Paray BA, Al-Sadoond MK (2018) Protective efficacy of Mucuna pruriens (L.) seed meal enriched diet on growth performance, innate immunity, and disease resistance in Oreochromis mossambicus against Aeromonas hydrophila. Fish Shellfish Immunol 75:374–380CrossRefGoogle Scholar
  41. Narnaware YK, Baker HN, Tomlinson MG (1994) The effect of various stress, corticosteroids and adrenergic agents on phagocytosis in the rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 13:31–34PubMedCrossRefGoogle Scholar
  42. Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29:2–14PubMedCrossRefGoogle Scholar
  43. Negm IM, El Asely AM, Abbass AA (2016) Influence of dietary ginger (Zingiber officinale) on haemato-biochemical parameters, spleen histopathological changes and resistance of Oreochromis niloticus fingerlings. Egyptian J Aquacult 6:25–45CrossRefGoogle Scholar
  44. Nishikimi M, Rao NA, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazinemethosulphate and molecular oxygen. Biochem Biophys Res Comm 46:849–854PubMedCrossRefGoogle Scholar
  45. NRC (2011) Nutrient requirement of fish and shrimp. Animal Nutrition Series. National Research Council of the National Academies. The National Academies Press, Washington, p 376Google Scholar
  46. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analyt Biochem 9:351–358CrossRefGoogle Scholar
  47. Ozovehe BN (2013) Growth performance, hematological indices and some biochemical enzymes of juveniles Clarias gariepinus [Burchell 1822] fed varying levels of Moringa oleifera leaf meal diet. J Aquat Res Devel 4:166–172Google Scholar
  48. Paglia DW, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169PubMedGoogle Scholar
  49. Puycha K, Yuangsoi B, Charoenwattanasak S, Wongmaneeprateep S, Niamphithak P, Wiriyapattanasub P (2017) Effect of moringa (Moringa oleifera) leaf supplementation on growth performance and feed utilization of Bocourti's catfish (Pangasius bocourti). Agricult. Nat Res 51:286–291Google Scholar
  50. Reverter M, Bontemps N, Lecchini D, Banaigs B, Sasal P (2014) Use of plant extracts in fish aquaculture as an alternative to chemotherapy: current status and future perspectives. Aquaculture 433:50–61CrossRefGoogle Scholar
  51. Richter N, Siddhuraju P, Becker K (2003) Evaluation of nutrition quality of Moringa (Moringa oleifera) leaves as an alternative protein Source for Nile tilapia (Orochromis niloticus L.). Aquaculture 217(1-4):599–611CrossRefGoogle Scholar
  52. Şahan A, Özütok S, Kurutaş EB (2016) Determination of some haematological parameters and antioxidant capacity in Nile tilapia (Oreochromis niloticus Linnaeus, 1758) fed ginger (Zingiber officinale Roscoe) to Aeromonas hydrophila. Turkish J Fish Aquat Sci 16:197–204Google Scholar
  53. Saini RK, Sivanesan I, Keum YS (2016) Phytochemicals of Moringa oleifera: A review of their nutritional, therapeutic and industrial significance. Biotech 6:203–217Google Scholar
  54. Schultz LA (1987) Methods in Clinical Chemistry. The C.V. Mosby Co., St. Louis, pp 742–746Google Scholar
  55. Sharma A, Deo AD, Tandel Riteshkumar S, Chanu TI, Das A (2010) Effect of Withania somnifera (L. Dunal) root as a feed additive on immunological parameters and disease resistance to Aeromonas hydrophila in Labeo rohita (Hamilton) fingerlings. Fish Shellfish Immunol 29:508–512PubMedCrossRefGoogle Scholar
  56. Sherif AH, El-Gamal AM, Tolan AE (2014) Incorporation of Moringa oleifera leaf in Nile tilapia Oreochromis niloticus diet and its effect on growth performance and immune status. J Vet Sci 1:806–814Google Scholar
  57. Sӧnmez AY, Bilen S, Alak G, Hisar O, Yanık T, Biswas G (2015) Growth performance and antioxidant enzyme activities in rainbow trout (Oncorhynchus mykiss) juveniles fed diets supplemented with sage, mint and thyme oils. Fish Physiol Biochem 41:165–175CrossRefGoogle Scholar
  58. Van Hai N (2015) The use of medicinal plants as immunostimulants in aquaculture: a review. Aquaculture 446:88–96CrossRefGoogle Scholar
  59. Woldehiwet Z, Rowan TG (1990) Some observations on the effects of age of calves on the phagocytosis and killing of Staphylococcus aureus by polymorphonuclear leucocytes. Brit Vet J 146:165–170CrossRefGoogle Scholar
  60. Zahran E, Abd El-Gawad EA, Risha E (2018) Dietary Withania sominefera root confers protective and immunotherapeutic effects against Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 80:641–650PubMedCrossRefGoogle Scholar
  61. Zhang C, Gong S, Yu D, Yuan H (2009) Propolis and herbaepimedii extracts enhance the non-specific immune response and disease resistance of Chinese sucker, Myxocyprinus asiaticus. Fish Shellfish Immunol 26:467–472PubMedCrossRefGoogle Scholar
  62. Zilberg D, Tal A, Froyman N, Abutbul S, Dudai N, Golan-Goldhirsh A (2010) Dried leaves of Rosmarinus officinalis as a treatment for streptococcosis in tilapia. J Fish Dis 33:361–365PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Aquatic Animals Diseases and Management, Faculty of Veterinary MedicineBenha UniversityBenhaEgypt
  2. 2.Institute of AquacultureUniversity of StirlingStirlingUK

Personalised recommendations