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Effect of dietary purslane (Portulaca oleracea L.) leaves powder on growth, immunostimulation, and protection of Nile tilapia, Oreochromis niloticus against Aeromonas hydrophila infection

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Abstract

A feeding trial was conducted to assess the effect of inclusion of dried powder of purslane, Portulaca oleracea, leaves in diets on growth, antioxidant, and immunological responses of Nile tilapia, Oreochromis niloticus, as well as its resistance to pathogenic bacteria, Aeromonas hydrophila. Fresh leaves of purslane were collected, dried, and mixed thoroughly with a basal fish diet at levels of 0.0 (control), 1.0, 2.0, and 3%. Fish (18.2 ± 0.4 g) fed one of the experimental diets up to apparent satiation twice a day for 7 weeks. At the end of the feeding trial, fish were intraperitoneally injected with pathogenic bacteria, A. hydrophila, and fish mortalities were observed and recorded up to 10 days post-challenge. Fish growth, weight gain, and specific growth rate were retarded significantly with increasing purslane levels in fish diets as compared to the control group. On the other hand, significant (P < 0.05) increases in plasmatic superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX) activities accompanied with significant decreases in malondialdehyde (MDA) were observed with increasing purslane levels in fish diets. The respiratory burst (RB) activity and lysozyme value were significantly enhanced, while nitrous oxide (NO) decreased significantly with increasing purslane levels in fish diets over those of the control fish. After 10 days of the bacterial infection, no significant changes of MDA and SOD levels were observed, whereas CAT and GPX activities were significantly elevated. Additionally, RB and lysozyme activities were lower, while NO levels were elevated more than those before bacterial infection. Fish survival before and after bacterial infection was significantly affected by dietary purslane supplements, bacterial infection, and their interaction where dietary purslane improved the fish resistance to A. hydrophila infection in a dose-dependent manner. Purslane-fed fish showed highest relative percent of survival especially at an inclusion level of 3% (81.25%), whereas the control fish group showed lowest relative percent of survival (0.0%).

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References

  • Abdel-Tawwab M (2016) Feed supplementation to freshwater fish: experimental approaches. Lambert Academic Publishing, Berlin

    Google Scholar 

  • Abdel-Tawwab M, Abbass FE (2017) Turmeric powder, Curcuma longa L., in common carp, Cyprinus carpio L., diets: growth performance, innate immunity, and challenge against pathogenic Aeromonas hydrophila infection. J World Aquacult Soc 48:303–312. https://doi.org/10.1111/jwas.12349

    Article  Google Scholar 

  • Abdel-Tawwab M, Ahmad MH, Seden MEA, Sakr SFM (2010) Use of green tea, Camellia sinensis L., in practical diet for growth and protection of Nile tilapia, Oreochromis niloticus (L.), against Aeromonas hydrophila infection. J World Aquacult Soc 41:203–213. https://doi.org/10.1111/j.1749-7345.2010.00360.x

    Article  Google Scholar 

  • Abdel-Tawwab M, Adeshina I, Jenyo-Oni A, Ajani EK, Emikpe BO (2018a) Growth, physiological, antioxidants, and immune response of African catfish, Clarias gariepinus (B.), to dietary clove basil, Ocimum gratissimum, leaf extract and its susceptibility to listeria monocytogenes infection. Fish Shellfish Immunol 78:346–354. https://doi.org/10.1016/j.fsi.2018.04.057

    Article  CAS  PubMed  Google Scholar 

  • Abdel-Tawwab M, Samir F, Abd El-Naby AS, Monier MN (2018b) Antioxidative and immunostimulatory effect of dietary cinnamon nanoparticles on the performance of Nile tilapia, Oreochromis niloticus (L.) and its susceptibility to hypoxia stress and Aeromonas hydrophila infection. Fish Shellfish Immunol 74:19–25

    CAS  PubMed  Google Scholar 

  • Adeshina I, Jenyo-Oni A, Emikpe BO et al (2019) Stimulatory effect of dietary clove, Eugenia caryophyllata, bud extract on growth performance, nutrient utilization, antioxidant capacity, and tolerance of African catfish, Clarias gariepinus (B.), to Aeromonas hydrophila infection. J World Aquacult Soc 50:390–405. https://doi.org/10.1111/jwas.12565

    Google Scholar 

  • Aebi H (1984) Methods in enzymology. Catalase Vitr 105:121–126

    CAS  Google Scholar 

  • Anderson DP (1992) Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annu Rev Fish Dis 2:281–307

    Google Scholar 

  • Anjugam M, Vaseeharan B, Iswarya A, Gobi N, Divya M, Thangaraj MP, Elumalai P (2018) Effect of β-1, 3 glucan binding protein based zinc oxide nanoparticles supplemented diet on immune response and disease resistance in Oreochromis mossambicus against Aeromonas hydrophila. Fish Shellfish Immunol 76:247–259

    CAS  PubMed  Google Scholar 

  • Awad NE (1994) Lipid content and antimicrobial activity of phenolic constituents of cultivated Portulaca oleracea L. Bull Fac Pharm Cairo Univ 32:137–142

    CAS  Google Scholar 

  • Bove PF, van der Vliet A (2006) Nitric oxide and reactive nitrogen species in airway epithelial signaling and inflammation. Free Radic Biol Med 41:515–527

    CAS  PubMed  Google Scholar 

  • Boyd CE, Tucker CS (2012) Pond aquaculture water quality management. Springer Science & Business Media, Kluwer Academic Publishers, Dordrecht

  • Carbone D, Faggio C (2016) Importance of prebiotics in aquaculture as immunostimulants. Effects on immune system of Sparus aurata and Dicentrarchus labrax. Fish Shellfish Immunol 54:172–178

    CAS  PubMed  Google Scholar 

  • Caruso D, Schlumberger O, Dahm C, Proteau J-P (2002) Plasma lysozyme levels in sheatfish Silurus glanis (L.) subjected to stress and experimental infection with Edwardsiella tarda. Aquac Res 33:999–1008

    Google Scholar 

  • Chakraborty SB, Hancz C (2011) Application of phytochemicals as immunostimulant, antipathogenic and antistress agents in finfish culture. Rev Aquac 3:103–119

    Google Scholar 

  • Chen D, Ainsworth AJ (1992) Glucan administration potentiates immune defence mechanisms of channel catfish, Ictalurus punctatus Rafinesque. J Fish Dis 15:295–304

    CAS  Google Scholar 

  • Dkhil MA, Moniem AEA, Al-Quraishy S, Saleh RA (2011) Antioxidant effect of purslane (Portulaca oleracea) and its mechanism of action. J Med Plant Res 5:1589–1593

    Google Scholar 

  • Dweck AC (2001) Purslane (Portulaca oleracea): the global panacea. Pers Care Manag 2:7–15

    Google Scholar 

  • Dytham C (2011) Choosing and using statistics: a biologist’s guide. Blackwell Science Ltd, London

  • Ellis AE (1990) Lysozyme assays. Tech fish Immunol 1:101–103

    Google Scholar 

  • Ellis AE (2001) Innate host defense mechanisms of fish against viruses and bacteria. Dev Comp Immunol 25:827–839

    CAS  PubMed  Google Scholar 

  • El-Sayed A-FM (2006) Tilapia culture. CABI publishing, CABI International Willingford, Oxfordshire, UK

  • Erkan N (2012) Antioxidant activity and phenolic compounds of fractions from Portulaca oleracea L. Food Chem 133:775–781

    CAS  Google Scholar 

  • Foster MW, Hess DT, Stamler JS (2009) Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med 15:391–404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galina J, Yin G, Ardo L, Jeney Z (2009) The use of immunostimulating herbs in fish. An overview of research. Fish Physiol Biochem 35:669–676

    CAS  PubMed  Google Scholar 

  • Geng AL, Guo YM, Yang Y (2004) Reduction of ascites mortality in broilers by coenzyme Q10. Poult Sci 83:1587–1593

    CAS  PubMed  Google Scholar 

  • Ghorbani MR, Bojarpur M, Mayahi M et al (2013) Effect of purslane (Portulaca oleracea L.) on blood lipid concentration and antioxidant status of broiler chickens. Online J Vet Res 17:54–63

    Google Scholar 

  • Gobi N, Vaseeharan B, Chen JC, Rekha R, Vijayakumar S, Anjugam M, Iswarya A (2018) Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol 74:501–508

    CAS  PubMed  Google Scholar 

  • Grinde B (1989) Lysozyme from rainbow trout, Salmo gairdneri Richardson, as an antibacterial agent against fish pathogens. J Fish Dis 12:95–104

    CAS  Google Scholar 

  • Haygood AM, Jha R (2018) Strategies to modulate the intestinal microbiota of tilapia (Oreochromis sp.) in aquaculture: a review. Rev Aquac 10:320–333

    Google Scholar 

  • Hermes-Lima M (2004) Oxygen in biology and biochemistry: role of free radicals. Funct Metab Regul Adapt 1:319–366

    Google Scholar 

  • Hozayen W, Bastawy M, Elshafeey H (2011) Effects of aqueous purslane (Portulaca oleracea) extract and fish oil on gentamicin nephrotoxicity in albino rats. Nat Sci 9:47–62

    Google Scholar 

  • Iranshahy M, Javadi B, Iranshahi M, Jahanbakhsh SP, Mahyari S, Hassani FV, Karimi G (2017) A review of traditional uses, phytochemistry and pharmacology of Portulaca oleracea L. J Ethnopharmacol 205:158–172

    CAS  PubMed  Google Scholar 

  • Islam MW, Zakaria MNM, Radhakrishnan R et al (1998) Evaluation of analgesic activity of the aerial parts of Portulaca oleracea V. sativa and its comparison with two related species. J Pharm Pharmacol 50:226–226

    CAS  Google Scholar 

  • Iswarya A, Vaseeharan B, Anjugam M, Gobi N, Divya M, Faggio C (2018) β-1, 3 glucan binding protein based selenium nanowire enhances the immune status of Cyprinus carpio and protection against Aeromonas hydrophila infection. Fish Shellfish Immunol 83:61–75

    CAS  PubMed  Google Scholar 

  • Jin S, Zhang H, Zhang B (2010) Effects of ethanol extract and water extract from the Porslane to bleeding-time and anti-hypoxia survival time in mice. J Med Sci Yanbian Univ 3:11

    Google Scholar 

  • Kehrer JP (1993) Free radicals as mediators of tissue injury and disease. Crit Rev Toxicol 23:21–48

    CAS  PubMed  Google Scholar 

  • Korni FMM, Khalil F (2017) Effect of ginger and its nanoparticles on growth performance, cognition capability, immunity and prevention of motile Aeromonas septicaemia in Cyprinus carpio fingerlings. Aquac Nutr 23:1492–1499

    CAS  Google Scholar 

  • Lan X, Dongming X, Wei W et al (2006) Review on chemical constituents of Portulaca oleracea L. Asia-Pac Tradit Med 7:35

    Google Scholar 

  • Leung AY, Foster S (1996) Encyclopedia of common natural ingredients used in food, drugs, and cosmetics. J Am Chem Soc 118:8988

    Google Scholar 

  • Li P, Wen Q, Gatlin DM III (2009) Dose-dependent influences of dietary β-1, 3-glucan on innate immunity and disease resistance of hybrid striped bass Morone chrysops x Morone saxatilis. Aquac Res 40:1578–1584

    CAS  Google Scholar 

  • Lim YY, Quah EPL (2007) Antioxidant properties of different cultivars of Portulaca oleracea. Food Chem 103:734–740

    CAS  Google Scholar 

  • Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151

    PubMed  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  PubMed  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    CAS  PubMed  Google Scholar 

  • Oliveira I, Valentão P, Lopes R, Andrade PB, Bento A, Pereira JA (2009) Phytochemical characterization and radical scavenging activity of Portulaca oleraceae L. leaves and stems. Microchem J 92:129–134

    CAS  Google Scholar 

  • Olson N, Van Der Vliet A (2011) Interactions between nitric oxide and hypoxia-inducible factor signaling pathways in inflammatory disease. Nitric Oxide 25:125–137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  PubMed  Google Scholar 

  • Pan J-Q, Tan X, Li J-C, Sun WD, Wang XL (2005) Effects of early feed restriction and cold temperature on lipid peroxidation, pulmonary vascular remodelling and ascites morbidity in broilers under normal and cold temperature. Br Poult Sci 46:374–381

    CAS  PubMed  Google Scholar 

  • Parry O, Marks JA, Okwuasaba FK (1993) The skeletal muscle relaxant action of Portulaca oleracea: role of potassium ions. J Ethnopharmacol 40:187–194

    CAS  PubMed  Google Scholar 

  • Rashed AN, Afifi FU, Disi AM (2003) Simple evaluation of the wound healing activity of a crude extract of Portulaca oleracea L. (growing in Jordan) in Mus musculus JVI-1. J Ethnopharmacol 88:131–136

    CAS  PubMed  Google Scholar 

  • Rook GAW, Steele J, Umar S, Dockrell HM (1985) A simple method for the solubilisation of reduced NBT, and its use as a colorimetric assay for activation of human macrophages by γ-interferon. J Immunol Methods 82:161–167

    CAS  PubMed  Google Scholar 

  • Ruiz MC (2017) Effects of purslane (Portulaca oleracea L.) and Shewanella putrefaciens probiotic enriched diet on gilthead seabream (Sparus aurata L). Msc in Aquaculture, Faculdade de Ciências e Tecnologia, Universidade do Algarve, Portgal

  • Sadeghi G, Karimi A, Shafeie F, Vaziry A, Farhadi D (2016) The effects of purslane (Portulaca oleracea L.) powder on growth performance, carcass characteristics, antioxidant status, and blood metabolites in broiler chickens. Livest Sci 184:35–40

    Google Scholar 

  • Samy J, Sugumaran M, Lee KLW (2009) Herbs of Malaysia: an introduction to the medicinal, culinary, aromatic and cosmetic use of herbs, Shah Alam, Selangor Darul Eshan, Malaysia

  • Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239

    CAS  Google Scholar 

  • Schäperclaus W (1992) Fish diseases. CRC Press Boca Raton, FL

  • Schmidt H, Kelm M (1996) Determination of nitrite and nitrate by the Griess reaction. In: Feelisch, M., Stamler, J.S. (Eds.), Methods in Nitric Oxide Research. Wiley, Brisbane, pp. 491–497

  • Simopoulos AP, Tan D-X, Manchester LC, Reiter RJ (2005) Purslane: a plant source of omega-3 fatty acids and melatonin. J Pineal Res 39:331–332

    CAS  PubMed  Google Scholar 

  • Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29:1715–1733

    CAS  PubMed  Google Scholar 

  • Uddin MK, Juraimi AS, Ali ME, Ismail MR (2012) Evaluation of antioxidant properties and mineral composition of purslane (Portulaca oleracea L.) at different growth stages. Int J Mol Sci 13:10257–10267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vaseeharan B, Thaya R (2014) Medicinal plant derivatives as immunostimulants: an alternative to chemotherapeutics and antibiotics in aquaculture. Aquac Int 22:1079–1091

    CAS  Google Scholar 

  • Xiang L, Xing D, Wang W, Wang R, Ding Y, du L (2005) Alkaloids from Portulaca oleracea L. Phytochemistry 66:2595–2601

    CAS  PubMed  Google Scholar 

  • Yang Z, Liu C, Xiang L, Zheng Y (2009) Phenolic alkaloids as a new class of antioxidants in Portulaca oleracea. Phyther Res An Int J Devoted to Pharmacol Toxicol Eval Nat Prod Deriv 23:1032–1035

    CAS  Google Scholar 

  • Yue T, Xiaosa W, Ruirui Q, Wencai S, Hailiang X, Min L (2015) The effects of Portulaca oleracea on hypoxia-induced pulmonary edema in mice. High Alt Med Biol 16:43–51

    PubMed  PubMed Central  Google Scholar 

  • Zhang XJ, Ji YB, Qu Z et al (2002) Experimental studies on antibiotic functions of Portulaca oleracea L. in vitro. Chin J Microecol 14:277–280

    Google Scholar 

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Funding

The current work has been funded by Central Laboratory for Aquaculture Research, Abbassa, Abo-Hammad, Sharqia, Egypt.

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Authors and Affiliations

  1. Department of Fish Health and Management, Central Laboratory for Aquaculture Research, Abbassa, Abo-Hammad, Sharqia, 44662, Egypt

    Nashwa Abdel-Razek & Somayah M. Awad

  2. Department of Fish Biology and Ecology, Central Laboratory for Aquaculture Research, Abbassa, Abo-Hammad, Sharqia, 44662, Egypt

    Mohsen Abdel-Tawwab

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  1. Nashwa Abdel-Razek
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  2. Somayah M. Awad
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  3. Mohsen Abdel-Tawwab
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Correspondence to Mohsen Abdel-Tawwab.

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The current study was complied with the ethical statements, which lays down minimum standards for protecting animals used in experimentation and for other scientific purposes and approved by Animal Ethics Committee of Agriculture Research Center, Giza, Egypt.

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Abdel-Razek, N., Awad, S.M. & Abdel-Tawwab, M. Effect of dietary purslane (Portulaca oleracea L.) leaves powder on growth, immunostimulation, and protection of Nile tilapia, Oreochromis niloticus against Aeromonas hydrophila infection. Fish Physiol Biochem 45, 1907–1917 (2019). https://doi.org/10.1007/s10695-019-00685-8

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