Abstract
Moringa oleifera is a highly nutritious and water purifier plant that is widely utilized in the aquaculture sector. Tilapia fish has various advantageous characteristics endowing it appropriate for aquaculture. Thus, this current study is designed to evaluate the impact of Moringa oleifera MOAE aqueous extract supplementation at the levels of 0, 100, 200, and 400 mg/kg diet for 3 months on Nile tilapia, Oreochromis niloticus. Antioxidant capacity, reproductive hormones, cytokines, and gonadal histological and caspase-3 immune-histochemical changes are assessed. Outcomes revealed a significant (P < 0.05) decrease in the antioxidant (CAT, SOD, GSH, and GPx) readings plus a significant (P < 0.05) increase in the proinflammatory cytokines (TNFα, IL1-β) was recorded for the 400 mg MOAE/kg group. In addition, significant (P < 0.05) improvements in estradiol and testosterone concentrations were detected in the 200 mg MOAE group. However, gonadal histological alterations were detected in the 400 mg MOAE/kg group, while the best histo-architectures were recorded for the 200 mg MOAE/kg group. Associated Caspase-3 immunoexpression showed wide-ranging positive three cells indicating severe apoptotic features for the 400 mg MOAE/kg group. Consequently, 200 mg/kg diet MOAE dietary supplementation is suggested for enhancing immune-antioxidant traits and reproductive hormones and modulating cytokines, as well as gonadal activity enhancement of O. niloticus with caution when the level of MOAE exceeds 200 mg/kg diet.
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No datasets were generated or analyzed during the current study. All data are available in this manuscript.
References
Abdel Rahman AN, Mahmoud SM, Khamis T et al (2022a) Palliative effect of dietary common sage leaves against toxic impacts of nonylphenol in mirror carp (Cyprinus carpio var specularis): growth, gene expression, immune-antioxidant status, and histopathological alterations. Aquac Rep 25:101200. https://doi.org/10.1016/j.aqrep.2022.101200
Abdel Rahman AN, Mansour DA, Abd El-Rahman GI et al (2022b) Imidacloprid toxicity in Clarias gariepinus: protective role of dietary Hyphaene thebaica against biochemical and histopathological disruption, oxidative stress, immune genes expressions, and Aeromonas sobria infection. Aquaculture 555:738170. https://doi.org/10.1016/j.aquaculture.2022.738170
Aebi H (1984) [13] Catalase in vitro. In: Methods in enzymology. Academic Press, pp 121–126
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). Aquac Res 34:1147–1159. https://doi.org/10.1046/j.1365-2109.2003.00920.x
Akin-Obasola B, Jegede T (2014) Histological analysis of female redbelly tilapia; Tilapia zillii (Gervais, 1848) ovary, fed bitter melon, Momordica charantia (Cucurbitaceae) leaf meal. J Agric Sci 6:p229. https://doi.org/10.5539/jas.v6n11p229
Alzahrani OM, Elumalai P, Nada HS et al (2023) Pseudomonas putida: sensitivity to various antibiotics, genetic diversity, virulence, and role of formic acid to modulate the immune-antioxidant status of the challenged Nile tilapia compared to carvacrol oil. Fishes. https://doi.org/10.3390/fishes8010006
Anhwange B, Ajibola VO, Oniye S (2004) Amino acids compositions of the seeds of Moringa oleifera (LAM) Detarium mirocarpum (Guill & Perr) Bauhinia monandra (Linn). ChemClass J 9–13
Anwar F, Rashid TDU (2007) Physiochemical characteristics of Moringa oleifera seeds and seed oil from a wild provenance of Pakistan. Pak J Bot 39:1443–1453
Ayotunde EO, Fagbenro OA, Adebayo OT (2011) Histological changes in Oreochromis niloticus (Linnaeus I779) exposed to aqueous extract of Moringa oleifera seeds powder. Turk J Fish Aquat Sci 11:37–43
Benli AÇK, Köksal G, Özkul A (2008) Sublethal ammonia exposure of Nile tilapia (Oreochromis niloticus L.): effects on gill, liver and kidney histology. Chemosphere 72:1355–1358. https://doi.org/10.1016/j.chemosphere.2008.04.037
Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888
Bharali R, Tabassum J, Azad MRH (2003) Chemomodulatory effect of Moringa oleifera, Lam, on hepatic carcinogen metabolising enzymes, antioxidant parameters and skin papillomagenesis in mice. Asian Pac J Cancer Prev APJCP 4:131–139
Cui C, Chen S, Wang X et al (2019) Characterization of Moringa oleifera roots polysaccharide MRP-1 with anti-inflammatory effect. Int J Biol Macromol 132:844–851. https://doi.org/10.1016/j.ijbiomac.2019.03.210
El-Kassas S, Aljahdali N, Abdo SE et al (2022) Moringa oleifera leaf powder dietary inclusion differentially modulates the antioxidant, inflammatory, and histopathological responses of normal and Aeromonas hydrophila-infected mono-sex Nile Tilapia (Oreochromis niloticus). Front Vet Sci 9:918933. https://doi.org/10.3389/fvets.2022.918933
Elabd H, Wang H-P, Shaheen A et al (2016) Feeding Glycyrrhiza glabra (liquorice) and Astragalus membranaceus (AM) alters innate immune and physiological responses in yellow perch (Perca flavescens). Fish Shellfish Immunol 54:374–384. https://doi.org/10.1016/j.fsi.2016.04.024
Elabd H, Wang H-P, Shaheen A et al (2017) Anti-oxidative effects of some dietary supplements on yellow perch (Perca flavescens) exposed to different physical stressors. Aquac Rep 8:21–30. https://doi.org/10.1016/j.aqrep.2017.09.002
Elabd H, Wang H-P, Shaheen A, Matter A (2020) Nano spirulina dietary supplementation augments growth, antioxidative and immunological reactions, digestion, and protection of Nile tilapia, Oreochromis niloticus, against Aeromonas veronii and some physical stressors. Fish Physiol Biochem 46:2143–2155. https://doi.org/10.1007/s10695-020-00864-y
Emam M, Farouk S, Abdo M (2018) The ameliorative potential of probiotics and/or silymarin on thioacetamide induced hepatotoxicity in rats: histological and immunohistochemical study. Int J Morphol 36:661–669. https://doi.org/10.4067/S0717-95022018000200661
Emam MA, Shourbela RM, El-Hawarry WN et al (2024) Effects of Moringa oleifera aqueous extract on the growth performance, blood characteristics, and histological features of gills and livers in Nile tilapia. Aquac Fish 9:85–92. https://doi.org/10.1016/j.aaf.2021.12.011
Fahey J (2005) Moringa oleifera: a review of the medical evidence for its nutritional, therapeutic, and prophylactic properties. Part 1. Trees Life J. https://doi.org/10.1201/9781420039078.ch12
FAO (2022) Understanding and implementing catch documentation schemes: a guide for national authorities. FAO, Rome, Italy
Gad EM, Abd El-Rahman A, Shalaby AM, Metwally SM (2019) Biochemical changes of Moringa seeds extracts on Nile tilapia breeding fish. Egypt J Aquac 9:77–95. https://doi.org/10.21608/eja.2019.48769
García Beltrán JM, Silvera DG, Ruiz CE et al (2020) Effects of dietary Origanum vulgare on gilthead seabream (Sparus aurata L.) immune and antioxidant status. Fish Shellfish Immunol 99:452–461. https://doi.org/10.1016/j.fsi.2020.02.040
Hamed HS, Amen RM, Elelemi AH et al (2022) Effect of dietary Moringa oleifera leaves nanoparticles on growth performance, physiological, immunological responses, and liver antioxidant biomarkers in Nile tilapia (Oreochromis niloticus) against zinc oxide nanoparticles toxicity. Fishes 7:360. https://doi.org/10.3390/fishes7060360
Ibrahem M, Fathi M, Ibrahim M, Ibrahim A (2013) The role of Spirulina platensis (Arthrospira platensis) in growth and immunity of Nile tilapia (Oreochromis niloticus) and its resistance to bacterial infection. J Agric Sci 5. https://doi.org/10.5539/jas.v5n6p109
Jabeen R, shahid muhammad, Jamil A, Ashraf M (2008) Microscopic evaluation of the antimicrobial activity of seed extracts of Moringa oleifera. Pak J Bot 40
Jaja-Chimedza A, Graf B, Simmler C et al (2017) Biochemical characterization and anti-inflammatory properties of an isothiocyanate-enriched moringa (Moringa oleifera) seed extract. PLoS ONE. https://doi.org/10.1371/journal.pone.0182658
Kalb D, Vo HD, Adikari S et al (2021) Visualization and modeling of inhibition of IL-1β and TNF-α mRNA transcription at the single-cell level. Sci Rep 11:13692. https://doi.org/10.1038/s41598-021-92846-0
Leone A, Spada A, Battezzati A et al (2015) Cultivation, genetic, ethnopharmacology, phytochemistry and pharmacology of Moringa oleifera leaves: an overview. Int J Mol Sci 16:12791–12835. https://doi.org/10.3390/ijms160612791
Liu H, Shen M, He Y et al (2023) Analysis of differentially expressed proteins after EHP-infection and characterization of caspase 3 protein in the whiteleg shrimp (Litopenaeus vannamei). Fish Shellfish Immunol 135:108698. https://doi.org/10.1016/j.fsi.2023.108698
Magray AR, Ganai BA, Ahmad F (2020) Isolation, identification and pathogenicity patterns of Mucor hiemalis in cultured Cyprinis carpio communis using challenged system. Aquaculture 518:734837. https://doi.org/10.1016/j.aquaculture.2019.734837
Mansour AT, Hamed HS, El-Beltagi HS, Mohamed WF (2022) Modulatory effect of papaya extract against chlorpyrifos-induced oxidative stress, immune suppression, endocrine disruption, and DNA damage in female Clarias gariepinus. Int J Environ Res Public Health 19:4640. https://doi.org/10.3390/ijerph19084640
Martins J, Leikoski N, Wahlsten M et al (2018) Sphaerocyclamide, a prenylated cyanobactin from the cyanobacterium Sphaerospermopsis sp. LEGE 00249. Sci Rep 8:14537. https://doi.org/10.1038/s41598-018-32618-5
Mohamed AA-R, El-Houseiny W, EL-Murr AE et al (2020) Effect of hexavalent chromium exposure on the liver and kidney tissues related to the expression of CYP450 and GST genes of Oreochromis niloticus fish: role of curcumin supplemented diet. Ecotoxicol Environ Saf 188:109890. https://doi.org/10.1016/j.ecoenv.2019.109890
Nishikimi M, Appaji Rao N, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854. https://doi.org/10.1016/S0006-291X(72)80218-3
Nouri M-Z, Kroll K, Webb M, Denslow N (2020) Quantification of steroid hormones in low volume plasma and tissue homogenates of fish using LC-MS/MS. Gen Comp Endocrinol 296:113543. https://doi.org/10.1016/j.ygcen.2020.113543
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169
Philip E, Eteng S, Nwosu F, Eyo V (2021) Comparative study of the growth and gonad development of Clarias gariepinus (Burchell 1822) fed diets with plant and animal-based ingredients in concrete tanks 13-Nov-2020 17-33-59. 2:1203–1210
Puycha K, Yuangsoi B, Charoenwattanasak S et al (2017) Effect of moringa (Moringa oleifera) leaf supplementation on growth performance and feed utilization of Bocourti’s catfish (Pangasius bocourti). Agric Nat Resour 51:286–291. https://doi.org/10.1016/j.anres.2017.10.001
Rashidian G, Mahboub HH, Fahim A et al (2022) Mooseer (Allium hirtifolium) boosts growth, general health status, and resistance of rainbow trout (Oncorhynchus mykiss) against Streptococcus iniae infection. Fish Shellfish Immunol 120:360–368. https://doi.org/10.1016/j.fsi.2021.12.012
Rohani MF, Islam SM, Hossain MK et al (2022) Probiotics, prebiotics and synbiotics improved the functionality of aquafeed: upgrading growth, reproduction, immunity and disease resistance in fish. Fish Shellfish Immunol 120:569–589. https://doi.org/10.1016/j.fsi.2021.12.037
Ruttarattanamongkol K, Petrasch A (2015) Antimicrobial activities of Moringa oleifera seed and seed oil residue and oxidative stability of its cold pressed oil compared with extra virgin olive oil. Songklanakarin J Sci Technol 37:587–594
Sakai M, Hikima J, Kono T (2021) Fish cytokines: current research and applications. Fish Sci 87:1–9. https://doi.org/10.1007/s12562-020-01476-4
Scapigliati G, Buonocore F, Bird S et al (2001) Phylogeny of cytokines: molecular cloning and expression analysis of sea bass Dicentrarchus labrax interleukin-1beta. Fish Shellfish Immunol 11:711–726. https://doi.org/10.1006/fsim.2001.0347
Sherif A (2014) Incorporation of Moringa oleifera in Nile tilapia Oreochromis niloticus diet and its effect on growth performance and immune status. J Vet Sci 1:806–814
Shourbela R, El-Hawarry W, A.M A SYA (2020) Potentiality of Moringa oleifera aqueous extract as a growth modulator and antistress in acute hypoxic Nile tilapia Oreochromis niloticus. Iran J Fish Sci 19:6784. https://doi.org/10.22092/ijfs.2019.119208
Soliva CR, Kreuzer M, Foidl N et al (2005) Feeding value of whole and extracted Moringa oleifera leaves for ruminants and their effects on ruminal fermentation in vitro. Anim Feed Sci Technol 118:47–62. https://doi.org/10.1016/j.anifeedsci.2004.10.005
Sreelatha S, Padma PR (2009) Antioxidant activity and total phenolic content of Moringa oleifera leaves in two stages of maturity. Plant Foods Hum Nutr 64:303–311. https://doi.org/10.1007/s11130-009-0141-0
Suvarna SK, Layton C, Bancroft JD (2019) Preface to the eighth edition. In: Suvarna SK, Layton C, Bancroft JD (eds) Bancroft’s theory and practice of histological techniques, 8th edn. Elsevier, p v
Waterman C, Cheng DM, Rojas-Silva P et al (2014) Stable, water extractable isothiocyanates from Moringa oleifera leaves attenuate inflammation in vitro. Phytochemistry 103:114–122. https://doi.org/10.1016/j.phytochem.2014.03.028
Xu Y-B, Chen G-L, Guo M-Q (2019) Antioxidant and anti-inflammatory activities of the crude extracts of Moringa oleifera from Kenya and their correlations with flavonoids. Antioxid Basel Switz 8:296. https://doi.org/10.3390/antiox8080296
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This work was supported by the Researches Supporting Project number (RSP2024R36), King Saud University, Riyadh, Saudi Arabia.
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Conceptualization: FG, ME, RS, EW, AA, SD, HM, HE. Methodology: FG, ME, RS. Formal analysis: FG, ME, RS, HE. Investigation: FG, ME, RS. Resources: EW, AA, SD. Writing—original draft preparation: FG, ME, RS, HM, HE. Writing—review and editing: ME, HM, HE. All the authors have read and agreed to the published version of the manuscript.
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Gad, Fm., Emam, M.A., Shourbela, R.M. et al. The influence of various doses of Moringa oleifera extract on the antioxidant trait, cytokines, reproductive hormones performance, and gonadal histological profiles of Nile tilapia. Aquacult Int (2024). https://doi.org/10.1007/s10499-024-01504-5
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DOI: https://doi.org/10.1007/s10499-024-01504-5